178
NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR SPINE TORSION Peter J. Fazey B.App.Sc. (PT), Grad.Dip.Manip.Ther. (Curtin), FACP Submitted in fulfilment of the requirements for the degree of Doctor of Philosophy July 2011 The Centre for Musculoskeletal Studies School of Surgery The University of Western Australia

NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

  • Upload
    others

  • View
    4

  • Download
    0

Embed Size (px)

Citation preview

Page 1: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

NUCLEUS PULPOSUS DEFORMATION

IN RESPONSE TO LUMBAR SPINE TORSION

Peter J. Fazey

B.App.Sc. (PT), Grad.Dip.Manip.Ther. (Curtin), FACP

Submitted in fulfilment of the requirements for the degree of Doctor of Philosophy

July 2011

The Centre for Musculoskeletal Studies

School of Surgery

The University of Western Australia

Page 2: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

ABSTRACT

Page i

Background

The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus

(AF) and the proteoglycan based, hydrophilic nucleus pulposus (NP). The primary role

of the NP is load attenuation which it achieves by deforming within the confines of the

anulus via a hydrostatic mechanism. The pattern of deformation is assumed to be away

from the position of offset loading. Changes in spinal posture result in variable loading.

Sagittal plane positioning has been shown to result in deformation of the NP towards

the convexity in most cases. Primary uniplanar lumbar segment movement results in

additional movement in a secondary plane. Spinal rotation, though small in range

intersegmentally, plays an important role in locomotion and contributes to multiplanar

motion and spinal flexibility. Rotation is also implicated as a common mechanism by

which the IVD may be injured. Few data exist reporting the direction of NP deformation

relative to rotated positions. Such information may inform the knowledge base on

injuring mechanisms and normal lumbar spine mechanics.

Purpose

The primary purpose of this thesis investigation was to quantify the in vivo effect of

rotation postures on lumbar NP deformation and to report the predictability of the

direction of that deformation. Additionally, the effects of coincident coronal plane

positions, age related changes and spinal deformity (scoliosis) were examined to

determine the relative influences of such factors on the internal mechanism of the IVD.

The principal hypothesis was that the NP would deform in all cases and conditions in a

predictable direction and with a magnitude proportional to the resultant segmental

angulation.

Methods

This investigation is divided into two main themes. The first describes the development

of a reliable methodology and reports normative data for NP deformation; the second

applies the methodology to subject populations with age changes in the IVD and

idiopathic scoliosis with a secondary lumbar curve. An initial ex vivo Computerised

Tomography (CT) based study examined the influence of joint morphology and IVD

degeneration on intersegmental rotation ranges. Three human osteoligamentous lumbar

Page 3: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Page ii

spines were placed in a purpose built torsion apparatus. Following application of axial

plane loading, displacements were tracked using a three dimensional motion analysis

instrument [Polhemius, Burlington, USA]. CT scanning was performed at incremental

loads and subsequently analysed for segmental rotation range and zygapophysial joint

gapping relative to disc pathology.

This study raised the question of the effect of rotation on IVD mechanics. Subsequently

a novel series of in vivo Magnetic Resonance Imaging (MRI) based studies were

devised to map hydration patterns and NP deformation in rotated positions of the

lumbar spine.

A pilot study (n=3), a normative rotation investigation (n=10) and normative lateral

flexion study (n=21) were conducted. All were undertaken with a substantially similar

methodology. Both T1 and T2 weighted lumbar MRI sequences were obtained in

sagittal plane positions with and without left trunk rotation. A pixel profile technique

was applied to the image data to determine direction and magnitude of NP deformation

at target intervertebral levels.

Data were derived using Image-J image analysis software (NIH, Bethesda, USA). Three

equidistant lines were placed across the mid disc region from which pixel data was

displayed, averaged in a Labview routine (National Instruments, Austin, USA) and

imported into Excel where direction and magnitude of NP deformation were compiled.

Intersegmental lateral flexion and rotation angles were measured and analysed for inter-

relationships with NP deformation.

To investigate the theme in non-normative populations, two cohort studies involving

subjects with age related IVD changes (n=11) and idiopathic scoliosis with secondary

lumbar curvature (n=12) were examined. Minor methodological refinements were made

to subject positioning and MRI slice angles to optimise segmental image and data

quality. The same image analysis method was applied to T1 and T2 weighted MRI

images to determine NP deformation patterns and directional predictability.

Page 4: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Page iii

Results

The cadaveric study reported greater ranges of axial rotation and joint separation in

lumbar segments in the presence of coronally oriented facets and degenerative disc

disease compared with sagitally oriented facets and discs without degenerative change.

The method used to gauge the deformation of the NP in different positions was

modified over the time course of the MRI studies and the following trends were

determined: (i) in normal young asymptomatic subjects positioned in the extremes of

flexion or extension within the MR imager, most NPs showed a tendency to deform

away from the area of greatest compression i.e. anteriorly in the case of lumbar

extension and to the convexity in the case of constrained lateral flexion, (ii) where

young subjects were positioned in left rotation plus either flexion or extension, there

was less certainty in predicting the deformation direction of the NP, (iii) there was

greater predictability of NP deformation direction relative to intersegmental lateral

flexion than axial rotation, (iv) in the case of older subjects with various stages of age

related disc disease, the trend was for similar NP deformation directional predictability

but reduced NP deformation magnitude and (v), in the case of the adolescents with

scoliosis all discs displayed a NP which deformed towards the concavity of the lateral

flexed apical disc segment.

Conclusions

The principal hypothesis that lumbar NP deformation direction was predictable relative

to positions in sagittal and coronal plane positions was accepted but was rejected for

axial plane positions. The magnitude of NP deformation was variable, being greater in

young subjects with well hydrated discs and less so in older IVDs with age related

changes and reduced hydration signal. The greatest NP deformation magnitude was seen

in the apical segments of secondary lumbar curves of subjects with the tri-dimensional

structural deformity of adolescent idiopathic scoliosis.

No relationships were evident between NP deformation magnitude and intersegmental

lateral flexion and rotation angles.

Page 5: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

STATEMENT OF ORIGINALITY

Page iv

This thesis is presented in complete fulfilment for the degree of Doctor of Philosophy at

the University of Western Australia, through the Centre for Musculoskeletal Studies,

The School of Surgery.

The research project was developed by the author in consultation with supervisors

Winthrop Professor Kevin Singer, Director of the Centre for Musculoskeletal Studies,

The School of Surgery, the University of Western Australia; Dr Roger Price, Head of

Department, Medical Technology and Physics, Sir Charles Gairdner Hospital, and

Adjunct Professor, School of Surgery, The University of Western Australia; and Dr

Swithin Song FRACR, Head of Department, Magnetic Resonance Imaging and

Radiology, Royal Perth Hospital, Western Australia, who have also contributed to

editing of this thesis.

Planning and management of this study was the sole responsibility of the author.

Recruitment of volunteers was jointly undertaken by the author and Winthrop Professor

Kevin Singer in accordance with University informed consent and ethical standards.

The author conducted all aspects of testing with the exception of radiology. The author

independently analysed all data in consultation with supervisors.

The material comprising this thesis is the original work of the author towards the PhD

degree, unless otherwise stated. This thesis has not been submitted, either in part in

whole, for the award of any other degree at this or any other University.

Peter Fazey

July, 2011

Page 6: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

ACKNOWLEDGEMENTS

Page v

Many People and organisations have contributed to the successful completion of this

thesis over an extended period. Thank you to all the individuals who volunteered to

participate in the numerous studies that comprise this thesis and those who, by way of

intelligent comment, opinion or passing remark, have unwittingly stimulated thoughts

that have shaped the direction of the thesis.

Paramount and heartfelt thanks must go to my primary supervisor Winthrop Professor

Kevin Singer for: his considerable patience and understanding of my extraneous

professional involvements; his continuous encouragement and reminding that the more

difficult and challenging times and tasks were indeed the most character forming; his

boundless patience in guiding and educating me along the research path – at times a

painfully slow and arduous journey for both; his facilitation of many aspects of all the

studies and the benefit of his extensive network, professional reputation and knowledge.

His vision alone was, thankfully, unwavering.

Thanks also to my secondary supervisor Adjunct Professor Roger Price whose rigorous

scientific and grammatical advice given with such good humour and gentle honesty

were both invaluable and greatly appreciated.

To co-supervisor Dr Swithin Song for his specific technical advice and facilitation of

access to the MRI unit at Royal Perth Hospital which was clearly fundamental to MRI

based research.

To Orthopaedic spinal surgeon Mr Peter Woodland for his continual, good natured

willingness to provide both clinical and editing advice as well as access to patient

records, his very professional and skilled staff, in particular orthotist Sandy Crameri,

and opening his spinal deformity clinic to me on many occasions.

To the brilliantly expert MRI technicians at Royal Perth Hospital, Barry Tanian and

Leonie Maddren for their considerable technical expertise and advice in developing the

MRI protocols given so freely and so early in the morning over weekends.

To Ray Smith for his technical and software advice and help, he always had the answer

and there was nothing he couldn’t fix.

Page 7: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Page vi

To my numerous co-authors in the various publications all contributed more than they

realise and made the whole greater than the sum of its parts. In particular Hiroshi

Takasaki, whose unstoppable drive was infectious and whose collaboration on several

publications invaluable. The thesis is greater as a result.

Finally, to Melissa whose support and continual encouragement motivated me when

nothing else could. This thesis is dedicated to her positivity and belief in me and is

testament to her strength and commitment.

Page 8: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

THESIS PUBLICATIONS

Page vii

This thesis contains three published co-authored papers, five manuscripts and three co-

authored text chapters; their location within the text is indicated.

1. Peer reviewed journal papers and manuscripts

Fazey PJ, with: Song S, Mønsås Å, Johansson L, Haukalid T, Singer KP (2006). An

MRI investigation of intervertebral disc deformation in response to torsion.

Clinical Biomechanics 21, 538-542 (Appendix 4)

Fazey PJ, with: Takasaki H, Singer KP (2010). Nucleus pulposus deformation in

response to lumbar spine lateral flexion: an in vivo MRI investigation. European

Spine Journal 19(7): 1115-20

Fazey PJ, with: Takasaki H, May S, Hall T (2010). Nucleus pulposus deformation

following application of mechanical diagnosis and therapy: a single case report

with magnetic resonance imaging. Journal of Manual and Manipulative Therapy

18(3): 153-158 (Appendix 5)

Fazey PJ, with: Svansson GR, Day R, Price RI, Singer KP (2011). Pathoanatomical

influences on segmental rotation in the lumbar spine: Association between CT

imaging and 3D motion tracking. Submitted.

Fazey PJ, with: Song S, Price RI, Singer KP (2011). Internal derangement of the

lumbar intervertabral disc in response to torsion. Submitted.

Fazey PJ, with: Song S, Price RI, Singer KP (2011). Nucleus pulposus deformation

relative to rotation in middle aged lumbar intervertebral discs. Submitted.

Fazey PJ, with: Woodland P, Song S, Price RI, Singer KP (2011). The contribution of

lumbar nucleus deformation to the deformity of scoliosis: A preliminary

investigation. Submitted.

Fazey PJ, with: Woodland P, Song S, Price RI, Singer KP (2011). Herniated nucleus

pulposus – a quantitative 12 year longitudinal case study of paravertebral muscle

changes. Submitted.

2. Book chapters

Fazey PJ, with: Singer KP, (2004) Disc herniation - nonoperative management. In: HK

Herkowitiz, J Dvorak, G Bell, M Nordin, D Grob [eds] ISSLS Lumbar Spine. 3e.

Raven Lippincott, Philadelphia. pp 427-436 (Appendix 6)

Fazey PJ, with: Singer KP, Boyle J, (2005) Comparative anatomy of the zygapophysial

joints of the spine. In: J Boyling & G Jull [eds]. Greive's Modern Manual Therapy

3e. Churchill Livingstone. Edinburgh. pp 187-201 (Appendix 7)

Page 9: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Page viii

Fazey PJ, with: Khan K, Singer KP, (2011) Thoracic and Chest Pain. In: K Khan & P

Brukner [eds]. Clinical Sports Medicine, 4e. McGraw-Hill Education Australia

and New Zealand. In Press (Appendix 11)

3. Conference presentations

Fazey, PJ, Rotation effects on the lumbar intervertebral disc. Australian Physiotherapy

Association WA state conference: Perth 2003

Fazey, PJ, Effects of torsion on the lumbar intervertebral disc. Musculoskeletal

Physiotherapy Australia, National conference: Sydney 2003

Fazey, PJ, Intervertebral disc deformation in response to torsion. Spine Society of

Australia biennial scientific meeting: Auckland, New Zealand 2005

Fazey, PJ, Intervertebral disc deformation in response to torsion. Musculoskeletal

Physiotherapy Australia Biennial National conference: Brisbane 2005 (Appendix

8)

Fazey, PJ, Does sustained lumbar rotation induce nucleus pulposus deformation in a

predicable manner ? – an MRI investigation. World Confederation for Physical

Therapy International Congress, Vancouver, Canada 2007.

Fazey, PJ, Nucleus Pulposus deformation in response to rotation – an in vivo MRI

investigation. 6th

International Meeting of Physical Therapy Science, Perth 2008.

Fazey, PJ, with: Song S, Price RI, Singer KP. Lumbar intervertebral disc deformation

in response to rotation: an age contrast study employing MRI. American Physical

Therapy Association National Conference, Baltimore 2009 (Appendix 9)

Fazey, PJ, with: Breidahl WH, Singer KP,Fatal fracture disclocations associated with

an ankylosed spine: A case report. Spine Society of Australia scientific meeting.

Adelaide, Australia 2009 (Appendix 10)

DECLARATION FOR THESIS CONTAINING PUBLISHED WORK

This thesis contains published co-authored work comprising chapters 4, 6 and 9 and

appendices 4 – 7. These papers and chapters were published during the course of

enrolment for this thesis investigation in collaboration with supervisors who provided

editorial advice and input in their submission for publication. As such the work

contained within these chapters was by greater majority the work of the author at

submission for publication.

Peter Fazey Professor Kevin Singer

PhD candidate Coordinating supervisor

Page 10: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

TABLE OF CONTENTS

Page ix

ABSTRACT.......................................................................................................................i

STATEMENT OF ORIGINALITY.................................................................................iv

ACKNOWLEDGMENTS.................................................................................................v

THESIS PUBLICATIONS..............................................................................................vii

TABLE OF CONTENTS.................................................................................................ix

LIST OF APPENDICES..................................................................................................xi

GLOSSARY OF ABBREVIATIONS.............................................................................xii

GLOSSARY OF DEFINITIONS...................................................................................xiii

CHAPTER 1

Introduction.....................................................................................................................I-1

CHAPTER 2

Review of Literature......................................................................................................II-1

CHAPTER 3

Methods........................................................................................................................III-1

CHAPTER 4

Pathoanatomical influences on segmental rotation in the lumbar spine: Association

between CT imaging and 3D motion tracking ............................................................IV-1

CHAPTER 5

Internal derangement of the lumbar intervertabral disc in response to torsion.............V-1

CHAPTER 6

Nucleus pulposus deformation in response to lumbar spine lateral flexion: an in vivo

MRI investigation........................................................................................................VI-1

CHAPTER 7

Nucleus pulposus deformation relative to rotation in middle aged lumbar intervertebral

discs............................................................................................................................VII-1

CHAPTER 8

The contribution of lumbar nucleus deformation to the deformity of scoliosis: A

preliminary investigation............................................................................................VII-1

CHAPTER 9

Herniated nucleus pulposus – a quantitative 12 year longitudinal case study of

paravertebral muscle changes....................................................................................VIII-1

Page 11: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Page x

CHAPTER 10

Discussion.....................................................................................................................X-1

CHAPTER 11

Conclusions and recommendations..............................................................................XI-1

APPENDICES

Page 12: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

LIST OF APPENDICES

Page xi

APPENDIX 1 Human Research and Ethics Committee application form

APPENDIX 2 Participant information and consent

APPENDIX 3 MRI consent form

APPENDIX 4 Fazey PJ, with: Song S, Mønsås Å, Johansson L, Haukalid T, Singer

KP (2006). An MRI investigation of intervertebral disc deformation in

response to torsion. Clinical Biomechanics 21, 538-542

APPENDIX 5 Fazey PJ, with: Takasaki H, May S, Hall T (2010). Nucleus pulposus

deformation following application of mechanical diagnosis and

therapy: a single case report with magnetic resonance imaging.

Journal of Manual and Manipulative Therapy 18(3): 153-158

APPENDIX 6 Fazey PJ, with: Singer KP, (2004) Disc herniation - nonoperative

management. In: HK Herkowitiz, J Dvorak, G Bell, M Nordin, D

Grob [eds] ISSLS Lumbar Spine. 3e. Raven Lippincott, Philadelphia.

pp 427-436

APPENDIX 7 Fazey PJ, with: Singer KP, Boyle J, (2005) Comparative anatomy of

the zygapophysial joints of the spine. In: J Boyling & G Jull [eds].

Greive's Modern Manual Therapy 3e. Churchill Livingstone.

Edinburgh. pp 187-201

APPENDIX 8 Fazey, PJ, Intervertebral disc deformation in response to torsion.

Musculoskeletal Physiotherapy Australia Biennial National

conference: Brisbane 2005

APPENDIX 9 Fazey, PJ, with: Song S, Price RI, Singer KP. Lumbar intervertebral

disc deformation in response to rotation: an age contrast study

employing MRI. American Physical Therapy Association National

Conference, Baltimore 2009

APPENDIX 10 Fazey, PJ, with: Breidahl WH, Singer KP,Fatal fracture disclocations

associated with an ankylosed spine: A case report. Spine Society of

Australia scientific meeting. Adelaide, Australia 2009

APPENDIX 11 Fazey PJ, with: Khan K, Singer KP, (2011) Thoracic and Chest Pain.

In: K Khan & P Brukner [eds]. Clinical Sports Medicine, 4e.

McGraw-Hill Education Australia and New Zealand. In Press.

Page 13: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

GLOSSARY OF ABBREVIATIONS

Page xii

A-P Antero-posterior

AF Anulus Fibrosus

CSA Cross Sectional Area

CT Computerised Tomography

CV Coefficient of Variation

FSU Functional Spinal Unit

HNP Herniated Nucleus Pulposis

IVD Intervertebral Disc

IVF Intervertebral Foramen

LBP Low Back Pain

LF Lateral Flexion

MRI Magnetic Resonance Imaging

mm Millimetre

MPa Megapascal

NP Nucleus Pulposus

P-A Postero-anterior

ROI Region of Interest

SF Side Flexion

US Ultrasonography

VB Vertebral Body

ZJ Zygapophysial Joint

Note: Anatomical spelling in this thesis is consistent with that listed in:

Terminologia Anatomica: International Anatomical Terminology, New York: Thieme

Medical Publishers, 1998.

The terms lateral flexion and side flexion are used interchangeably in this thesis.

Page 14: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

GLOSSARY OF DEFINITIONS

Page xiii

Arthrokinematics: Refers to articular mechanics (Williams et al., 1989). It typically

describes the direction and characteristics of movement or component parts of

movements of joints.

Axial rotation: Refers to the movement of a vertebral segment around the ‘y’ axis. The

direction is taken as that of a vertebral segment relative to its subjacent neighbour

(White & Panjabi, 1990).

Coupled (conjunct) movement: Occurs when rotation or translation about or along one

axis is consistently associated with rotation or translation about or along a second axis

(White & Panjabi, 1990). It is described in terms of direction.

Creep: Time dependent tissue deformation while under constant load. It usually occurs

as water is gradually expelled from the loaded tissue (White & Panjabi, 1990).

Deformation: Refers to a change in form or shape of a body. In the context of this

thesis with reference to the nucleus pulposus (NP) it refers to a change in NP shape

resulting from load application.

Directional predictability: In the context of this thesis this concept refers to how

predictably the nucleus pulposus will deform in a given direction within the confines of

the anulus.

Extension: Refers to regional spinal motion or segmental rotation or position in a

posterior direction from a given starting point. It includes both posterior segmental

rotation and posterior translation.

Flexion: Refers to regional spinal motion or segmental rotation or position in an

anterior direction from a given starting point. It includes both anterior segmental

rotation and anterior translation.

Page 15: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Page xiv

Hydration pattern: Refers to the variable distribution of hydration throughout a

prescribed region. In the context of this thesis that region is the intervertebral disc.

Lateral Flexion: Refers to regional spinal motion or segmental rotation or position in

the coronal plane from a given starting point. The terms lateral flexion and side flexion

are used synonymously.

Migration: Refers to the movement or displacement of material from one location to

another.

Osteokinematics: The study of bone movement (Williams et al., 1989). It is described

relative to standard axes or adjacent structures.

Spinal segmental Instability: The loss of the ability of the spine under physiologic

loads to maintain its pattern of displacement so that there is no initial or additional

neurological deficit, no major deformity, and no incapacitating pain (White and Panjabi,

1990, p278).

Common biomechanical terms are used throughout the thesis with reference to the

standard text, White and Panjabi, 1990.

White A, Panjabi M. Clinical Biomechanics of the Spine, 2 ed. Philadelphia: Lippincott,

1990.

Williams PL, Warwick R, Dyson M, Bannister LH. Gray's Anatomy, Edinburgh:

Churchill Livingstone, 1989.

Page 16: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

CHAPTER 1

Page I-1

Introduction

Low back pain (LBP) is highly prevalent in the community with an 85% lifetime and

35% point prevalence (Nachemson, 1999). Back pain is frequently attributed to

disorders of the intervertebral disc (IVD) (Gunzburg et al., 1991; van Tulder et al.,

2000) including degenerative change and internal disruptions of the disc resulting in

herniation. These may occur subsequent to acute injury or gradually due to repeated

minor trauma or age (Bogduk & Twomey, 1987). One mechanism of injury that is

commonly proposed involves rotary or twisting motions, often in combination with

loading of the spine (Farfan et al., 1972).

Intersegmental lumbar rotation is primarily limited by the orientation of the articular

facets and the collagenous fibre orientation of the anulus. The central region or nucleus,

is normally well-hydrated and behaves as a hydrostatic mechanism (Buckwalter, 1995).

Compression causes the nucleus pulposus (NP) to alter from a spherical shape to an

ovoid conformation (Adams et al., 1996). This exerts a circumferential pressure on the

walls of the surrounding collagen rings of the anulus fibrosus (AF), evenly distributing

the load across the disc and vertically to adjacent vertebral bodies via the end-plates. It

is also apparent that the NP, in response to asymmetric loading, will migrate toward the

area of least load (Krag et al., 1987; Kramer, 1981). Discs can undergo age-related

degeneration, with associated reduction in the degree of hydration (Modic & Ross,

2007). This jeopardises the effectiveness of load distribution, often causing abnormal

localised concentration of disc pressure which may result in ruptured or herniated discs,

or disruption of the vertebral end-plates. Consequently, IVD investigations employing

detailed imaging modalities and assessment of hydration will assist in ascertaining the

status of disc condition as it affects internal mechanics.

Many studies have been published on sagittal movement, and somewhat less on lateral

flexion; there is, however, a paucity of literature on the effects of rotation on internal

IVD mechanics and no reports of the effects of rotation on nucleus position or

deformation .

Page 17: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 1 – Introduction

Page I-2

Reports in the literature of migration of NP material within the confines of the AF

boundaries may not capture internal fluid redistribution within the NP and resultant NP

deformation. This subtle but important difference is elaborate in Chapter 10, section

10.2.1, pX-2.

The IVD exhibits time and rate-dependent and viscoelastic biomaterial properties. It is

assumed that mechanical loads in different positions influence the morphology and

internal structure of the IVD (White & Panjabi, 1990). Back exercises and passive

movement techniques have been prescribed on the basis of this concept (Cyriax &

Cyriax, 1993; McKenzie, 1981). McKenzie (1981) recommends the use of lumbar

extension exercises on the basis that the NP is purported to migrate anteriorly, thereby

distancing the NP from pain sensitive structures in an injured posterior anulus fibrosus.

Moreover, flexion exercises are believed to enlarge the cross sectional area of the neural

canal and intervertebral foramina, thereby decreasing mechanical stimulus of pain

sensitive structures contained within (White & Panjabi, 1990).

The trend towards an anterior NP migration following sagittal movements has also been

supported in several in vivo Magnetic Resonance Imaging (MRI) studies (Brault et al.,

1997; Edmondston et al., 2000; Fennell et al., 1996). However, the trend has not always

been consistent and segmental variations are reported (Edmondston et al., 2000; Fennell

et al., 1996). These studies have also used a variety of techniques to isolate and define

the NP or its boundaries, ranging from visual inspection to profiling the MRI pixel

intensity. This latter method, while effectively measuring hydration levels and

distribution, is limited to a single image sample of the IVD in one plane only and may

not represent accurately the total hydration distribution within the entire IVD.

Migration of the NP within the IVD in response to load distribution during axial

rotation remains unknown. However, rotation is assumed to change the foraminal

dimension by decreasing width and area on the ipsilateral side and increasing the

foraminal space on the contralateral side (Fujiwara et al., 2001). Nevertheless, the

mechanism of rotation is more complex as the concept of coupled movement must be

considered. Axial rotation is always combined with some degree of lateral flexion

(Pearcy et al., 1984). In the normal spine, rotation and lateral flexion are usually

coupled to the same side in flexion, whereas this coupling occurs to opposite sides in

Page 18: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 1 – Introduction

Page I-3

neutral and spinal extension (Pearcy & Tibrewal, 1984). Some authors claim coupled

motion at the lumbosacral junction occurs in the opposite manner and that at L4-5

coupling may vary unpredictably between individuals (Vicenzino & Twomey, 1993).

The direction of lateral flexion coupling may influence compression distribution within

the IVD, and consequently direction of NP migration during rotation. It is also reported

that segmental morphology influences axial rotation range according to different

positions within the range of available sagittal postures (Pearcy & Hindle, 1991).

This thesis aims to examine the effect of rotation on the intervertebral disc with

reference to the relationship between axial and coronal rotation via a series of unique in

vivo studies of intradiscal hydration patterns.

Improved understanding of the effects of rotation in vivo will contribute original

insights to the body of knowledge relevant to both aetiology and management of the

debilitating and costly condition that is low back pain.

In this study it is hypothesised that:

1. The nucleus pulposus will deform with rotation in a predictable fashion as a

function of coupled motion in normal individuals;

2. This model can be elaborated in physiological lateral flexion positions, and in

established scoliosis;

3. The reliability of predicting NP deformation in older individuals will be less

certain, dependent on the degree of established disc degeneration.

The primary study series was designed to generate hypotheses and raise questions

leading to subsequent more detailed investigations.

Part 1 of this thesis begins with a description of the methods employed through the

studies contained within (chapter 3). This includes explanation of the subtle

refinements to the methods made through the course of conducting the studies, as

development of the concept and testing of the hypotheses highlighted additional

variables and improved ways to examine the questions. The individual studies begin

with chapter 4 which describes the hypothesis generating study; a computerised

tomography (CT) ex vivo cadaveric evaluation of the biomechanics of axial rotation

Page 19: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 1 – Introduction

Page I-4

which considers pathoanatomical influences of degeneration relative to the IVD and

articular facet orientation. This is followed by an introduction to a novel method of

examining in vivo intradiscal hydration patterns utilising pixel intensity profiles derived

from Magnetic Resonance Imaging (MRI) and employs this to assess the intradiscal

effect of positional change relative to segmental rotation within sagittal, coronal and

axial planes in a cohort of young asymptomatic subjects (chapter 5). Chapter 6

examines in more detail the effect of a primary positioning in the coronal plane on NP

deformation, indexed by hydration pattern changes in the NP.

Part 2 integrates this understanding of biomechanics and intradiscal change into the

context of spinal pathology. Chapter 7 introduces the variable of age-related

degenerative change and its influence on predictability of rotation induced NP

deformation direction and magnitude. Chapter 8 evaluates NP deformation in

secondary lumbar curves of subjects with idiopathic scoliosis which includes deformity

in both the coronal and axial planes. Chapter 9 focuses on a single case study

subsequent to a lumbar rotation induced IVD trauma, with sequential imaging and

analysis over an extended period of recovery.

Chapter 10 discusses the results in context and draws common themes and trends

together while also acknowledging limitations in both method and results which qualify

the conclusions that may be drawn. Chapter 11 summarises and draws conclusions

which help inform the recommendations for future related studies and further questions

raised.

Following this introduction chapter 2 provides an overview of the background

literature relevant to parts 1 and 2 of this thesis.

Page 20: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 1 – Introduction

Page I-5

References

Adams MA, McNally DS, Dolan P. 'Stress' distributions inside intervertebral discs: the

effects of age and degeneration. The Journal of Bone and Joint Surgery Br 1996;

78(6): 965-72.

Bogduk N, Twomey L. Clinical Anatomy of the Lumbar Spine. London: Churchill

Livingstone, 1987.

Brault J, Driscoll D, Laakso L, Kappler R, Allin E, Glonek T. Quantification of lumbar

intradiscal deformation during flexion and extension by mathematical analysis

of magnetic resonance imaging pixel intensity profiles. Spine 1997; 22: 2066-

72.

Buckwalter JA. Aging and degeneration of the human intervertebral disc. Spine 1995;

20(11): 1307-14.

Cyriax H, Cyriax P. Illustrated Manual of Orthpaedic Medicine. Oxford: Butterworth

Heineman, 1993.

Edmondston S, Song S, Bricknell R, Davies P, Fersum K, Humphries P, Wickendon D,

Singer K. MRI evaluation of lumbar spine flexion and extension in

asymptomatic individuals. Manual Therapy 2000; 5: 158-64.

Farfan HF, Huberdeau RM, Dubow HI. Lumbar intervertebral disc degeneration: the

influence of geometrical features on the pattern of disc degeneration - a post

mortem study. J Bone Joint Surg Am 1972; 54(3): 492-510.

Fennell A, Jones A, Hukins D. Migration of the nucleus pulposus within the

intervertebral disc during flexion and extension of the spine. Spine 1996; 21:

2753- 7.

Fujiwara A, An H, Lim TH, Haughton V. Morphologic Changes in the Lumbar

Intervertebral Foramen Due to Flexion-Extension, Lateral Bending, and Axial

Rotation: An In Vitro Anatomic and Biomechanical Study. Spine 2001; 26(8):

876-82.

Gunzburg R, Hutton W, Fraser R. Axial rotation of the lumbar spine and the effect of

flexion. An in vitro and in vivo biomechanical study. Spine 1991; 16(1): 22-8.

Krag M, Seroussi R, Wilder D, Pope M. Internal Displacement Distribution from In

Vitro Loading of Human Thoracic and Lumbar Spinal Motion Segments:

Experimental Results and Theoretical Predictions. Spine 1987; 12(10): 1001-7.

Kramer J. Intervertebral disc diseases. Causes, diagnosis, treatment and prophylaxis. .

Chicago: Year Book Medical Publishers, Inc, 1981.

McKenzie RA. The Lumbar Spine. Mechanical Diagnosis and Therapy. Wellington:

Spinal Publications, 1981;

Modic MT, Ross JS. Lumbar degenerative disk disease. Radiology 2007; 245(1): 43-61.

Nachemson A. Back Pain: Delimiting the problem in the next millenium. International

Journal of Law and Psychiatry 1999; 22: 473-90.

Pearcy M, Hindle R. Axial rotation of lumbar intervertebral joints in forward flexion.

Proc Inst Mech Eng [H] 1991; 205(4): 205-9.

Pearcy M, Portek I, Shepherd J. Three-dimensional x-ray analysis of normal movement

in the lumbar spine. Spine 1984; 9(3): 294-7.

Pearcy M, Tibrewal S. Axial rotation and lateral bending in the normal lumbar spine

measured by three-dimensional radiography. Spine 1984; 9: 582-87.

van Tulder M, Malmivaara A, Esmail R, Koes B. Exercise Therapy for Low Back Pain:

A Systematic Review Within the Framework of the Cochrane Collaboration

Back Review Group. Spine 2000; 25(21): 2784-96.

Vicenzino G, Twomey L. Sideflexion and induced lumbar spine conjunct rotation and

its influencing factors. Australian Journal of Physiotherapy 1993; 39: 299-306.

Page 21: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 1 – Introduction

Page I-6

White A, Panjabi M. Clinical Biomechanics of the Spine, 2 ed. Philadelphia: Lippincott,

1990.

Page 22: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

CHAPTER 2

Page II-1

Review of Literature

2.1 Overview

This literature review is divided into three sections. Section 1 will introduce the

relevant anatomy and physiology of the lumbar vertebral column as it relates to motion.

It includes a review of biomechanics of the lumbar region, with a focus on rotation, the

concept of complex coupled motion and IVD mechanics. Section 2 examines the

literature relevant to age related changes and degeneration of the spine and how that

impacts upon the biomechanics elaborated in Section 1. Section 2 also discusses other

pathologies in which mechanics are altered such as scoliosis and herniated nucleus

pulposus. Section 3 discusses imaging relative to investigations reported through the

body of the thesis in addition to the measurement techniques that have been employed

to analyse medical images. A summary of the review follows which highlights those

key questions arising from the literature which are subsequently investigated through

the thesis.

The literature reviewed in this chapter is confined largely to that which relates directly

to the subsequent thesis investigations.

2.1 Section 1: Anatomy, Physiology and Biomechanics

2.1.1 Anatomy

As form and function are intimately related, the purpose of this section is to review

basic spinal anatomy, knowledge of which is fundamental to an understanding of

function and mobility, including rotation. It is not intended to provide a comprehensive

review of spinal anatomy, rather it is restricted to those anatomical aspects relevant to

the study presented in this thesis. For a more thorough review of lumbar spine anatomy

the reader is directed to standard texts (Bogduk, 2005; Bogduk & Twomey, 1991).

The human spine is designed to provide stability while maintaining functional mobility

of both the axial and appendicular skeletons. In doing so it must also efficiently transmit

force and momentum during motion, especially ambulation. It has developed particular

anatomical dimensions and characteristics specific to mammals that equip it for bipedal

Page 23: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 2: Review of Literature

Page II-2

activity (Boszczyk et al., 2001). The spine is divided into three regions cervical,

thoracic and lumbar which integrate functionally despite markedly different roles.

The lumbar spine comprises five vertebrae and their intervening discs, each contributing

to the roles of rigidity and mobility. The functional unit of the lumbar spine (Figure 2.1)

comprises two adjacent vertebrae, the intervening intervertebral disc and endplates, the

paired zygapophysial joints, all adjoining ligaments, adjacent muscles and includes the

contents of the spinal canal, intervertebral foramen and areas between transverse and

spinous processes, (Schmorl & Junghanns, 1959).

Figure 2.1: An axial cryosection through L3-4 depicting the paired zygapophysial

joints, the adjacent intervertebral disc, and associated pre- and post-ventral musculature.

The anular layers of the disc are shown along with remnant neural elements of the cauda

equina within the dura. [AF = anulus fibrosus; P = psoas; M = multifidus; D = dura; Z =

zygapophysial joint]. (Image used with permission from: Dr G.Groen, University of

Utrecht, The Netherlands).

AF P

M

Z

D

Page 24: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 2: Review of Literature

Page II-3

2.1.1.2 The bony vertebra

To meet its cardinal role of rigidity, the lumbar vertebra comprises the vertebral body

(VB) anteriorly and the neural arch posteriorly.

To resist compression the VB consists of a cortical shell to constrain marrow and

cancellous bone and is essentially rectangular and semi lunar in lateral and transverse

sections respectively. The concave outer shell of cortical bone is strengthened by an

internal architecture of struts (trabeculae) running both vertically and horizontally. The

outer rim of the superior and inferior surfaces is of smoother bone called the ring

apophysis – a secondary ossification centre of the vertebral body (Schmorl &

Junghanns, 1959). The posterior column, connected to the anterior via the pedicles,

comprises the laminae, spinous process, transverse processes and articular facets, or

zygapophysial joints. The motion control function of the articular facets will be

discussed separately in section 2.1.2.2.

2.1.1.3 The intervertebral disc

The intervertebral disc is situated in the interbody space. It consists of the anulus

fibrosus, the nucleus pulposus and the vertebral end plates. The latter bound the disc

superiorly and inferiorly with predominantly hyaline cartilage approximately 1mm

thick. With a horizontal lamellar arrangement the end plates serve to contain the fluid

nucleus and provide a pathway for nutrient transfer between the spongiosa and the

central disc via small vascular buds (Giles & Singer, 1997).

The anulus contains 10 – 20 concentric rings of circumferential collagenous lamellae.

Type 1 collagen predominates in the periphery and Type 2 centrally. The peripheral

fibres connect the ring apophyses above and below while the central fibres act as a

meshwork capsule to contain the nucleus (Schollum et al., 2008). The lamellar fibres are

angled obliquely at approximately 65° to the sagittal plane. Each adjacent lamella is

oriented in the opposite direction to its neighbour. The oblique orientation places the

fibres optimally to resist torsion and translation (Bullough, 2007) (Figure 2.2). The

degree to which the anulus does so is arguable with respect to torsion especially in

flexion, the combination of which is reported to afford greater resistance to radial tears

(Veres et al., 2010a, b). Recently described radial connections between lamellae have

been suggested to play a role in nucleus pulposus biomechanics (Schollum et al., 2009).

Page 25: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 2: Review of Literature

Page II-4

The nerve supply to the intervertebral disc is meager and predominantly concentrated in

the periarticular connective tissue and central endplate (Fagan et al., 2003).

Figure 2.2: Anulus lamellae are oriented to resist translation and torsion (From

Bullough 2007)

2.1.1.4 The nucleus pulposus

The nucleus pulposus’ primary function is load attenuation. The NP consists of (in order

of magnitude) water, proteoglycans and a loose collagen matrix. Its fluid properties

disperse axial load to the periphery to brace the inner anular fibres. The nucleus behaves

as a hydrostatic mechanism deforming towards the area of least compression (Keyes &

Compere, 1932; McKenzie & May, 2003). How it deforms in response to torsion in

vivo is unclear. Normal IVD height (approximately 10mm) is largely maintained as a

function of the fluid filled nucleus and varies with diurnal loading (Malko et al., 1999).

Fluid loss with compressive loading occurs primarily in the posterior anulus (30%) and

the NP (15%) (McMillan et al., 1996). Proportional content and function of the

ultrastructure of the IVD as described by Lundon and Bolton are summarized in Table

2.1 (Lundon & Bolton, 2001).

2.1.1.5 The articular facets

The articular facets of adjacent vertebrae interlock to form the synovial zygapophysial

joints. These primarily control and limit motion into rotation and anterior translation

and also accept a minority weightbearing role in erect standing (Adams & Hutton, 1980;

Shirazi-Adl, 1991). Loading is increased with increasing extension moment between the

tip of the inferior articular process and the pars interarticulares of the subjacent level

(Yang & King, 1984). The articular surfaces are oriented more sagitally in the cranial

lumbar segments and progressively coronally in the more caudal. A concomitant medial

orientation ensures joint surface compression resists anterior translation during flexion.

Partial disengagement occurs in flexion exposing the inferior articular surface which

remains protected by a synovial fold.

Page 26: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 2: Review of Literature

Page II-5

Segmental axial rotation results in compression of the contralateral inferior facet against

the contralateral superior facet of the subjacent level. Simultaneously the ipsilateral joint

space widens thereby tensioning the joint capsule.

Sagittal facetal orientation constrains axial rotation to a greater extent than coronal

orientation (Haughton et al., 2002; Krismer et al., 1996; Singer et al., 2001).

Facet asymmetry is common. The definition of excessive asymmetry, or ‘tropism’, is

arbitrary but has been attempted mathematically (Boden et al., 1996). Tropism has been

investigated for its relationship with disc herniation (Karacan et al., 2004; Ko & Park,

1997; Lee et al., 2006; Park et al., 2001) and degenerative change (Boden et al., 1996;

Grogan et al., 1997; Murtagh et al., 1991; Newton et al., 1993; Noren et al., 1991;

Vanharanta et al., 1993).

Findings vary as to whether tropism predisposes to degenerative change however it has

been correlated with disc pathology including prolapse (Farfan & Sullivan, 1967). This

is likely difficult to assess due to the common and multifactorial nature of degenerative

change in the lumbar spine.

Lumbar facets develop symmetrically in children with a variation in joint maturity age

between genders. Females cease development at age 12 while males continue to develop

beyond this age. This differs from the thoracic spine where asymmetry is common in

children and attributed to the influence of upper limb activities (Masharawi et al.,

2008a; Masharawi et al., 2008b). This influence is dramatically less in the lumbar spine

putatively due to its relative distance from the upper limbs. Consequently development

of facet asymmetry is suggested to be a post adolescence occurrence (Masharawi et al.,

2009). Reichmann, however, reported that some adult joint features are present at birth

implying a prenatal genesis for the process of development (Reichmann, 1971b).

Tropism should not influence the ability of the facets to constrain segmental rotation.

However the more sagittally oriented facet would take the greater compressive force

under torsion strain and fail before an adjacent coronally oriented facet in ex vivo

failure load experimentation (Adams et al., 2002).

2.1.1.6 Muscles of the lumbar region

The muscles of the spine can be divided regionally into deep, intermediate and

superficial. It is the intermediate and deep layers that relate specifically to the lumbar

Page 27: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 2: Review of Literature

Page II-6

spine. The intermediate layer consists primarily of the erector spinae group. This

comprises iliocostalis, longissimus and spinalis. The erector spinae group arises from

the iliac crests, the posterior sacrum, the sacral and inferior lumbar spinous processes

and the supraspinous ligament. Their primary action is to extend the spine but acting

unilaterally may laterally flex the spine. These muscles may also contribute via motion

coupling (refer section 2.1.2.3) to rotation, though the direction would be variable

(Moore, 1997).

The deep layer comprises multifidus and rotatores. Multifidus has both unisegmental

and polysegmental fascicles arising from the mammillary process of one vertebra and

extending to the spinous process of an adjacent vertebra or one up to several segments

distant. It is an extensor of the spine but may unilaterally contribute to rotation towards

that side. Multifidus has also been ascribed a segmental stabilizing role (MacDonald et

al., 2009; Richardson et al., 2002). Rotatores arises from transverse processes and

extends to the junction of the lamina and transverse process of the level above. It will

also assist rotation ipsilaterally (Lee et al., 2005).

There also exists a minor deep layer of small intersegmental muscles; interspinales and

intertransversarii. The former attaches to adjacent spinous processes and the latter to

adjacent transverse processes. Interspinales has been implicated in extension and

rotation while intertransversarii is a lateral flexor and therefore, by default through

coupled motion, also a rotator (Bogduk & Twomey, 1987).

Other than the muscles described that have attachment directly to the spine there are

other rotators of the trunk that can generate considerable torque and as such induce

segmental rotation in vivo. These include the oblique abdominals and latissimus dorsi.

Little literature reports the segmental effect of large torque producing muscles though it

is reported in elite sports (Burnett et al., 2008; Burnett et al., 1998).

Page 28: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 2: Review of Literature

Page II-7

TABLE 2.1. Ultrastructure of the normal intervertebral disc.

Structure/component

Water Proteoglycans (PGs) Collagen Elastin Cells

Nucleus Pulposus

(NP)

70-90% 65% dry weight of NP

PGs are key to the inherent

mechanical prop

erties of the NP

PGs present in the NP

include hyaluronic acid,

chondroitin sulfate, and

keratan sulfate

15-20% dry weight

Exists as an irregular

network that binds PGs

Types II (85%) and small

amounts of types III,V,I

and XI collagens are found

in the NP

Small quantities of fibres with

no specific orientation

Chondrocytes (responsible

for production of matrix

including PGs and collagen

components)

Concentration of chondrocytes

in the NP is less than that of

the surrounding AF, and they

are found mainly in the

vertebral end plate area

Anulus Fibrosus

(AF)

60-70% 15-20% of dry weight of

AF

PG gel, together with cells

and elastin, occupies

the spaces between

the collagen fibers of the

lamellae of the AF; this

acts to bind the lamellae

together and contributes

to the stiffness of the AF

50-60% dry weight of AF

Type I (predominant

collagen of AF providing

resistance to tension) and

types II,III,V,VI and IX are

found in the AF

Concentration of type II

collagen progressively

increases towards the

centre of the anulus as type

I collagen concentration

decreases

10% of dry weight of the AF

Fibres are arranged in a

circular, oblique and vertical

manner within the lamellae

Elastin fibres are closely

related to the densely packed

collagen fibres; they are

oriented parallel to those fibres

Elastin confers

resilience/elasticity to AF

Chondrocytes and fibroblasts

are dispersed among the

collagen fibres of the

individual lamellae and

between the lamellae

themselves

Fibroblasts are found

predominantly in the

periphery of the AF;

chondrocytes towards the NP

Adapted from Lundon and Bolton, 2001

Page 29: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 2: Review of Literature

Page II-8

2.1.1.7 Axial rotation

The design features of the spine appear to be biased towards limitation and control of

axial rotation. While this may be necessary to avoid the deleterious effects of excessive

rotation it is also of benefit in trunk motion and translation of energy. Farfan has

postulated that by limiting rotation the spine is able to more effectively transmit force

generated by arm and shoulder swinging to the pelvis and lower limbs, thereby

powering ambulation (Farfan, 1973, 1995). Intersegmental torsion in the flexed position

is reported to increase nucleus pressure and the anulus’ resistance to radial tears by

approximately 50% (Veres et al., 2010a).

The extent to which the various anatomical structures limit rotation has been argued in

the literature. While it is claimed that the facets are the primary restraint to rotation

(Adams & Hutton, 1981a) the nucleus is also reported as providing the greatest

percentage of rotary stability (White & Panjabi, 1990). Earlier work (Farfan et al., 1970)

has suggested that microfailure of anular fibres at 3° of intersegmental rotation indicates

the major role of the anulus in rotation limitation. Later Adams and Hutton (1983b),

disputed this assertion, claiming that the primary anatomical restraint is in fact the

articular facets, since anular failure does not occur until 9° of rotation (Adams &

Hutton, 1983b).

Gunzburg et al (1992) have reported the role of capsuloligamentous structures in axial

rotation following sequential ex vivo lesioning and conclude that zygapophysial joint

capsules contribute to axial rotation constraint in flexion but that the posterior anulus

and posterior longitudinal ligaments are the primary restraint in flexion (Gunzburg et

al., 1992).

The posterior anulus is also reportedly afforded protection in rotation by the sagittal

configuration of the facet surfaces and in flexion by the capsular ligaments (Adams &

Hutton, 1983b).

The anatomy of the lumbar spine and the inextricable link between form and function

indicate a need to permit controlled rotation. Clearly there must exist a balance from

which optimal mechanical benefit and sufficient control to avoid injury will be derived.

Page 30: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 2: Review of Literature

Page II-9

2.1.2 Biomechanics

This section addresses only the literature relevant to the biomechanical principles

referred to in this thesis, in particular that which relates to axial rotation. For a more

detailed description of spinal biomechanics the reader is directed to the definitive texts

(Adams et al., 2006; White & Panjabi, 1990).

2.1.2.1 Osteokinematics

The bony vertebra rotates around x,y and z axes. This is accompanied by translatory

motion along a horizontal plane (Figure 2.3). Normal ranges of rotation in each plane

have been measured with stereographic radiography (Dvorak et al., 1991; Miles &

Sullivan, 1961; Pearcy et al., 1984; Pearcy & Tibrewal, 1984; Reichmann, 1971a) and

MRI with or without fluoroscopy (Haughton et al., 2002; Li et al., 2009; Xia et al.,

2009) segmentally (Yamamoto et al., 1989) as well as regionally (Russell et al., 1993).

In vivo and ex vivo segmental ranges are comparable in the published literature.

Axial rotation occurs about an axis through the posterior one third of the IVD. The

segmental range is dependent upon facet orientation; increasing with greater coronal

bias (Haughton et al., 2002; Singer et al., 2001; Singer et al., 1989; Singer et al., 1996).

Figure 2.3: Axes and directions of rotation and translation of lumbar vertebra (Adapted

from Bogduk & Twomey, 1987).

Page 31: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 2: Review of Literature

Page II-10

Ex vivo studies of unilateral rotation to failure demonstrate a migration of the rotational

axis towards the contralateral facet when torsion load is taken beyond physiological

limits (Adams & Hutton, 1981a; Wachowski et al., 2009). Failure typically occurs at the

compressed facet in the first instance (Farfan et al., 1970).

Ranges of axial rotation vary with sagittal plane positioning. Mid range flexion is

associated with marginally increased ranges (Pearcy et al., 1984; Pearcy & Tibrewal,

1984; Pearcy, 1993) while end range extension or full flexion is associated with reduced

ranges (Burnett et al., 2008; Pearcy & Hindle, 1991b). Likely this is due to the locking

of articular facets at the end range of extension, the relative unlocking in mid range

flexion and the re-locking at end range flexion where translation forces the medially

inclined facets against their subjacent partner.

It has, however, also been demonstrated that maximal decreased axial twist stiffness and

increased axial twist angle occur in maximal flexion (Drake & Callaghan, 2008). This

finding does not support the claim for greater motion in mid range flexion but may

reflect a discrepancy between segmental ex vivo and regional in vivo studies.

Pressurisation of the nucleus in an ex vivo study of isolated ovine disc constructs was

associated with tears of the outer anulus at the end plate junction in flexed specimens

and between the inner anulus and end plate in neutrally positioned segments (Veres et

al., 2010b). The relevance of this injury pattern to human in vivo conditions is unclear.

Translation typically occurs in the direction of segmental rotation about the x and z

axes. In primary axial rotation about the y axis, translation may occur in the direction of

coupled z axis rotation (refer Figure 2.3).

2.1.2.2 Arthrokinematics

A functional spinal unit (FSU) comprises two vertebra and the intervening intervertebral

disc and surrounding ligaments and muscles (refer section 2.1.1). The articular

components are considered to be the paired synovial posterior zygapophysial joints and

the interbody joint. The latter will be considered in more detail elsewhere in this thesis

in consideration of the intervertebral disc mechanics.

Page 32: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 2: Review of Literature

Page II-11

Anterior vertebral rotation causes the inferior articular facets to ride cranially on the

superior articular facets of the vertebra below (Stokes, 1988). This shear movement is

limited by compression of the anterior anulus and stretch of the zygapophysial joint

capsule. The capacious nature of the capsule superiorly and inferiorly allows

considerable movement (Singer et al., 2004). The articular surfaces are left somewhat

exposed but are protected by meniscoid inclusions; a fold of synovium that resides in

the polar recesses of the articular surfaces.

Posterior rotation results in caudal glide of the inferior articular facets on their

neighbour. This is limited by contact between the tip of the inferior articular process and

the lamina of the vertebra below (Adams & Hutton, 1980).

Axial rotation widens the intervertebral foramen (IVF) (Fujiwara et al., 2001) and

zygapophysial joint space on the ipsilateral side and compresses on the contralateral.

The thicker posterior portion of the lumbar zygapophysial joint capsule helps resist

excessive torsion (Singer et al., 2004) (Appendix 7).

Articular asymmetry of the zygapophysial joints, or ‘tropism’, occurs at the cervico-

thoracic junction (Boyle et al., 1996) and most commonly at the lumbo-sacral and

thoraco-lumbar junctions (Singer et al., 2004). Tropism may predispose the segment to

rotation towards the coronally oriented side during torsion coupled with posteroanterior

shear force.

For a detailed examination of zygapophysial joint anatomy the reader is directed to

Appendix 7.

2.1.2.3 Coupled motion

Coupled motion occurs when primary motion in one plane induces motion in another

(Lovett, 1905). It is a well documented and accepted mechanical property of the spine

(Cholewicki et al., 1996; White & Panjabi, 1990). The key literature on lumbar spine

coupling considers the relationship between lateral flexion and axial rotation; for every

degree of axial rotation there occurs approximately two degrees of lateral flexion

(Panjabi, 1989).

Controversy exists as to the direction of coupling in the lumbar spine (Cholewicki et al.,

1996). Some report a predominant contralateral pattern (Russell et al., 1993; Steffen et

Page 33: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 2: Review of Literature

Page II-12

al., 1997) while Vicenzino and Twomey (1993) claim a mixed pattern with segmental

variation.

Most studies investigating coupled motion are ex vivo and postulate that geometry

accounts for coupling directional preference (Scholten & Veldhuizen, 1985). Clearly

this does not consider the influence of contractile element action. In vivo evidence

exists to claim a predominant ipsilateral pattern which varies between maximal and sub

maximal voluntary contraction of trunk rotators (Ng et al., 2001). The lumbar extensor

muscles reportedly contribute only 5% of axial torque in the trunk; the majority being

attributed to the oblique abdominal group (Macintosh et al., 1993).

Finite element modeling has been used by Little et al (2008) to compare in vivo with ex

vivo three dimensional motion coupling. This study has confirmed consistency for all

primary motions except lateral bending concluding that coupling patterns occur due to

the anatomy of the osteoligamentous spine, however in lateral flexion the active

structures (muscles) play a key role.

Insertion of Steinman pins into thoracolumbar spinous processes of living subjects has

also been used to assess range of motion (Gregersen & Lucas, 1967) and coupling

(Steffen et al., 1997). Large variations between individuals were noted.

Coupling patterns are reportedly stronger in younger subjects and lateral flexion was

strongly associated with flexion (Russell et al., 1993).

Small amounts of coupling between lateral flexion and axial rotation clearly do occur in

the lumbar spine however the direction remains controversial.

Recent comprehensive reviews of the literature find no clear consensus with respect to

direction of coupling and caution against assumption (Harrison et al., 1998; Legaspi &

Edmond, 2007).

Coupling varies between segments and individuals as well as ex vivo and in vivo

conditions. Further investigation is merited to clarify patterns and the predisposing

factors to each type of motion.

Page 34: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 2: Review of Literature

Page II-13

2.1.2.4 The role of the intervertebral disc

The intervertebral disc’s primary function of load attenuation is achieved through the

predominant use of a hydrostatic mechanism (Adams et al., 2002; Adams et al., 1994;

Adams & Hutton, 1983a; Giles & Singer, 1997).

The NP will generally deform towards the convexity in response to offset compressive

loading (Adams et al., 2000; Beattie et al., 1994; Brault et al., 1997; Edmondston et al.,

2000; Fazey et al., 2006; Fennell et al., 1996; Périé et al., 2003; Périé et al., 2001). In a

well hydrated disc this pattern is typically the case however there are exceptions

reported in the literature where deformation occurs towards the concavity (Edmondston

et al., 2000; Fennell et al., 1996).

Most studies examining NP migration in sagittal positioning have supported the theory

that the NP will migrate posteriorly in forward flexion and anteriorly in extension

(Brault et al., 1997; Edmondston et al., 2000; Fazey et al., 2006; Fennell et al., 1996).

These authors have used a variety of methods including visual inspection and

measurement, mapping of pixel intensity and tracking of peak pixel intensity. All have

measured NP migration from sagittal images in that plane alone except Fazey et al

(2006) who measured NP deformation from axial images and in both coronal and

sagittal planes.

These studies examine NP migration, which conceptually must involve measurable

movement of its boundaries within the anulus. While this may be possible within a

compromised anulus, an IVD with an intact inner anulus would contain the NP so as to

allow minimal movement. As such it would be more appropriate to describe this as

representing deformation of the NP. This implies redistribution of fluid content within

an intact anulus in response to compressive force gradients across the disc. Measuring

NP migration alone would potentially not capture deformation and risks overlooking

marked force related change.

It has been reported by Edmondston et al (2000) that occasional individual subjects

exhibit anterior migration in flexion. While this may be due to the discrepancy between

migration and deformation it may also be due to posterior anular tensile forces

exceeding compressive forces anteriorly. This possibility has not been considered in the

literature. Posterior migration in extension would be more easily explained as the

Page 35: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 2: Review of Literature

Page II-14

posterior elements protect the posterior anulus from excessive compressive force in

extension (Adams et al., 2000).

There is a dearth of literature reporting NP deformation in response to torsion. The sole

report in healthy volunteers was by Fazey et al (2006), where directionality of

deformation was noted to be variable in the coronal plane (Fazey et al., 2006). There has

been limited reporting of NP deformation in the scoliotic spine by Périé (2001, 2003).

Anular bulging is reported to increase anteriorly and decrease posteriorly in flexion

(Adams et al., 2002), however this is challenged in a more recent in vivo MRI study that

reports bulge reduction both anteriorly and posteriorly (Parent et al., 2006b). The former

cites ex vivo studies that include axial loading while the latter reports from in vivo MRI

images obtained in unloaded flexion and extension. This may explain the discrepant

findings. A study employing similar methodology but in an open magnet MRI reported

reduction in posterior bulge on flexion, a finding which supports the ex vivo studies

(Lee et al., 2009).

Intradiscal pressure has been measured during positions such as recumbent lying,

sitting, standing and forward bending (Nachemson, 1960; Wilke et al., 1999). While

limited to primarily sagittal positioning, these studies confirm that pressure increases

occur predictably and in a graded fashion concomitantly with increasingly loaded

postures, from lying through standing and flexion to sitting. Pressures are reduced in

degenerate discs putatively due to the reduced hydrostation (Sato et al., 1999).

Positional anular compressive forces have been measured however not tensile forces.

Controversy exists with respect to pressure changes during in vivo axial rotation. Wilke

et al (1996) reported increased pressure, as did Adams et al (2002), however van

Deursen et al (2001) reported decreased intradiscal pressure in an ex vivo porcine

model, while Yantzer et al (2007) claims no effect. No clear consensus has emerged to

date.

Despite claims that the IVD has self sealing properties it may be that the measurement

technique employing needle pressure transducers interrupts the intradiscal environment

and alters intradiscal pressure unpredictably. This theory is supported by a recent report

Page 36: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 2: Review of Literature

Page II-15

of increased incidence of degenerative change in a 10 year follow up of patients having

undergone discography (Carragee et al., 2009). The increased incidence of degeneration

is putatively ascribed to the interruption to the internal disc homeostasis.

Loading the lumbar spine into flexion has been demonstrated to reduce intradiscal fluid

content particularly in the NP (Adams & Hutton, 1983a). This occurs when fluid

transfer occurs through both the peripheral anulus and the central portion of the end-

plate. Simulated diurnal changes in IVD volume have been reported using MRI (Malko

et al., 1999). After sustained loading, subjects demonstrated a mean recovery of 5.4% of

disc volume on supine lying for 3 hours. Volume changes relative to torsion have not

been measured.

Many of the studies on IVD material properties have been conducted ex vivo. This may

explain the variations and inconsistencies. The properties of cadaveric material are

affected by death, cooling and post mortem frozen storage. Despite these changes being

small (Adams et al., 2002) ex vivo studies do not permit exploration of the unknown

physiological variables of a fully functioning organism such as the influence of muscle

function and vascularity.

Recent development of imaging and other techniques capable of accurate in vivo

measurements will ultimately elucidate mechanisms in human volunteers which include

the influences of all relevant physiological systems; muscular, neural, articular and

vascular.

2.1.2.5 Mechanical limits of torsion

The IVD exhibits time-dependent and viscoelastic properties. Sustained loading causes

collagenous tissue to deform over time (creep) accounting for about 25% of disc height

loss. Intervertebral disc creep continues to occur over several hours. Sustained

compressive load has been shown to reduce fluid content of the IVD by 18% in

cadaveric specimens over six hours (McMillan et al., 1996). An in vivo MRI study

reported a 5.4% reduction in total disc volume after three hours of compressive loading

(Malko et al., 1999). In contrast, paraspinal tissues subjected to sustained loading

demonstrate most creep effect in a few minutes (Yahia et al., 1991).

Page 37: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 2: Review of Literature

Page II-16

Adjacent anular lamellae are weakly bound and can be pulled apart easily (Schollum et

al., 2008). In the plane of the anulus tensile strength is greater. Small samples in ex vivo

experiments will fail at 1-3 MPa (Adams et al., 2002).

Anular fibres exhibit normal stress strain curves typical of any biological tissue. Early

changes in the stress strain curve have been interpreted as microfailure at 3° of axial

rotation (Farfan et al., 1970). This is now considered to represent straightening of crimp

within anular fibres and failure is reported at much higher ranges (12°) (Bogduk &

Twomey, 1987). Rotational forces may stretch anular fibres by up to 7% (Stokes, 1987).

Deliberate sequential lesioning of facets and unidirectional anular fibres has concluded

that anular fibres are more capable of resisting torsion than the articular facets at lower

torques up to 8.5 Nm (Krismer et al., 1996). At higher torque values resistance by the

facet joints dominate (Adams & Hutton, 1981b). According to Farfan et al (1970)

following facetectomy, anular fibres fail macroscopically at torsion ranges between 11°

and 32°. Other ex vivo studies have noted facet fracture precedes anular rupture (Adams

& Hutton, 1981b).

2.2 Section 2: Degeneration and structural deformity

2.2.1 Degeneration

Considerable literature has been devoted to degeneration of the spine and its various

component parts. The classic paper by Keyes and Compere (1932) and the more recent

studies by Boos et al (2002) provide important reviews. It is beyond the scope of this

thesis to comprehensively review all such literature. Instead, a focus will be directed at

those aspects of degenerative change that influence the IVD’s response to torsion.

2.2.1.1 Morphology

Morphological changes occur progressively in the normal ageing spine. The terms

ageing and degeneration are used interchangeably in the literature and variably given

disease status by the use of the diagnostic term ‘degenerative disc disease’. It could be

argued that normal age related changes should not be considered a disease.

Age changes have been distinguished from degenerative changes by the preservation of

disc height (Twomey & Taylor, 1985).

Page 38: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 2: Review of Literature

Page II-17

2.2.1.2 Age changes

Changes attributable to ageing typically commence in the nucleus with a reduction in

proteoglycan production and concentration and therefore hydration. Non enzymatic

glycation causes brown pigmentation of the NP (Figure 2.4B). Cartilaginous endplates

show similar changes (Jensen et al., 2009; Modic & Herfkens, 1990) which may

compromise nutrient supply.

Functionally the NP loses pliancy, volume and hydrostatic capability. Its response to

mechanical stimulus would consequently be altered however there is little examination

of this within the literature relative to torsion.

Figure 2.4: Age changes of the NP. Normal well hydrated NP (A) Glycation causes

brown pigmentation (B) and loss of NP hydration permits inward buckling of anulus (C)

and endplate disruption (D) (Photographs from Adams et al, 2002).

2.2.1.3 Degeneration of the intervertebral disc

Degenerative change of the IVD may occur at any age (Modic & Ross, 2007). While

such change may commence in the second decade of life (Boos et al., 2002; Nerlich et

A

B

C

D

Page 39: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 2: Review of Literature

Page II-18

al., 1997) its increased frequency in older discs results in the inevitable linking with

ageing. Age related changes are usually concomitant with gross structural change in the

anulus and end plate and may begin in the nucleus (Haefeli et al., 2006). Anular changes

include radial tears, concentric clefts between lamellae (delamination), buckling of the

inner anulus and rim lesions (Adams et al., 2002).

All of these compromise the intradiscal environment and therefore the ability of the disc

to attenuate load and behave in a predictable manner (Modic & Ross, 2007).

Diffusion changes across the end plate and nucleus have been associated with reduced

nutrition and degenerative disc disease (Rajasekaran et al., 2010; Roberts et al., 1996).

End plate changes include local and generalised sclerosis, irregularity, Schmorls nodes

and bone marrow changes. The latter, or Modic changes, present as types 1, 2 or 3

(Modic & Ross, 2007). Table 2.2 describes the changes observed on T1 and T2

weighted MRI for each type of Modic change. Low signal on T1 weighted images is

associated with inflammation and increased back pain incidence High signal indicates

fatty marrow associated with stability indicating fusion. The relationship between end

plate or marrow signal changes and the response to torsion is unknown.

Modic changes are reported to convert from one type to another and represent different

stages of the same process (Mitra et al., 2004b; Vital et al., 2003; Zhang et al., 2008)

and have been associated with low back pain, degeneration and stability (Luoma et al.,

2009; Modic, 2007; Rahme & Moussa, 2008). Evaluation of Modic changes has

demonstrated good inter tester and excellent intra tester reliability (Fayad et al., 2009;

Peterson et al., 2007a; Zhang et al., 2008).

Table 2.2: Marrow changes on MRI in degenerative disc disease

T1 weighted T2 weighted Marrow status Significance

Type 1 Low (black) High (white) Fibrovascular Back pain, hypermobility

Type 2 High (white) High (white) Fatty Stability

Type 3 Low (black) Low (black) Fibrovascular Back pain, hypermobility

From: Rowe (1997)

Page 40: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 2: Review of Literature

Page II-19

The literature is consistent with respect to Modic changes and their relationship with

degeneration however there remains controversy over the relationship with low back

symptoms (Jensen et al., 2008; Peterson et al., 2007b; Rahme & Moussa, 2008).

Discs exhibiting degenerative change and radial tears have been shown to contain

granulation tissue and neovascularisation. Accompanying the vascular in-growth are

nociceptive nerve fibres, thereby rendering the degenerate disc more pain sensitive

(Freemont et al., 1997). Discogenic pain has been postulated to be linked to damage to

the outer anulus (Fraser et al., 1993) consistent with its innervation being largely

nociceptive (Fagan et al., 2003). Induced tears of the anular periphery may precipitate

degenerative changes involving the entire intervertebral disc (Osti et al., 1990). A model

of disc degeneration incorporating causative factors and changes at molecular,

microscopic and macroscopic levels, and as displayed by imaging has been proposed

(Figure 2.5) (Hadjipavlou et al., 2008).

Increased ranges of segmental axial rotation in the lumbar spine have been linked with

degenerative change (Haughton et al., 2002) and concordant pain on discography

(Blankenbaker et al., 2006). Rohlman (2006) using finite element modeling, reported

increased axial rotation range in mild degeneration but decreased ranges in more

severely degenerated discs (Rohlmann et al., 2006).

2.2.2 Structural deformity involving the intervertebral disc

The most common structural spinal deformity that includes a rotational component is

scoliosis. The pathogenesis of scoliosis is unknown though likely to be multifactorial

(Kouwenhoven & Castelein, 2008). There are numerous classifications of scoliosis, the

most common being idiopathic (Reamy & Slakey, 2001). The deformity is tri-

dimensional with changes in coronal, axial and sagittal planes (Wright, 2000). While

deformity was traditionally assessed from plain Xray the advent of axial imaging has

sparked interest in the axial rotation component (Kuklo et al., 2005). The rotational

component has a demonstrated association with the coronal deformity as the degree of

segmental rotation can predict coronal imbalance postoperatively (Behensky et al.,

2007). This is reasonable given the existence of coupled motion in the spine, however

segmental axial rotation has been demonstrated not to be altered by lateral flexion as it

would in the normal spine (Beuerlein et al., 2003). The rotational deformity occurs in

Page 41: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 2: Review of Literature

Page II-20

both the disc (55%) and the vertebral body (45%) (Birchall et al., 2005; Liljenqvist et

al., 2002).

Anulus Fibrosus Nucleus Pulposus Vertebral Endplate

Molecular cross-linking altered PGs

altered pH

dehydration

altered PGs

Microscopic Delamination, tears,

fissures, Fibrosus

Cracks, tears,

fractures

Thickening, cracks

Biomechanical Stiffening, increased

stress

depressurised Weakening, bowing

Imaging osteophytes Reduced signal

Figure 2.5: A simple model of disc degeneration. Multiple causative influences

interrupt the balance between synthesis and degradation of the matrix and are expressed

as features at molecular, microscopic and biomechanical levels

(From: Hadjipavlou et al, 2008).

Ageing Genetics Nutrition Metabolic Infection Mechanical

Degradation Synthesis

Matrix

Chondrocyte

Page 42: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 2: Review of Literature

Page II-21

2.3 Section 3: Imaging and measurement

2.3.1 History of spinal imaging

Since the discovery of Xrays in 1895 there have been many advances in technology and

technique to refine the diagnostic capabilities of musculoskeletal imaging. Introduction

of water based contrast in 1963 led to myelogram and the ability to image neural

structures in the spine (Sofka & Pavlov, 2009). The advent of cross sectional imaging –

Computerised Tomography (CT), Magnetic Resonance Imaging (MRI) and

Ultrasonography (US) – has made visualization of exquisite anatomic detail possible.

Clinicians now have at their disposal an array of options for imaging the spine including

plain Xray, discography, myelography, CT and CT myelography, MRI and nuclear

scintigraphy.

The literature has varied recommendations for the use of imaging, from being

mandatory for a patient with a suspected disc lesion (DePalma & Rothman, 1970) to

only if the results obtained will change treatment (Boden, 1996). False positives and

false negatives are common as imaging alone cannot identify a pain generating

structure. Provocative discography is the putative exception though this has also been

challenged (Carragee & Alamin, 2001; Carragee et al., 2009; Feydy et al., 2009).

2.3.2 Imaging types and their limitations

2.3.2.1 Plain Xray

Each type of spinal imaging has its uses and limitations. Plain radiographs have limited

value beyond identification of overt bony injury or deformity (Sofka & Pavlov, 2009;

Wright, 2000). Observation of changes in adjacent structures may allow an indirect

assessment for example, reduction in disc space and osteophytosis is reported to infer

disc degeneration although direct visualization of the disc is not possible (Malfair &

Beall, 2007).

2.3.2.2 Stereoradiography

Stereoradiography is used primarily for motion analysis in two planes and was popular

in the 1980s (Dvorak et al., 1991; Pearcy et al., 1984; Pearcy & Tibrewal, 1984). Recent

use has been in digital form for 3 dimensional reconstruction (Rousseau et al., 2007).

Page 43: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 2: Review of Literature

Page II-22

2.3.2.3 Computerised Tomography (CT)

While CT visualizes soft tissue, neural structures and IVD more clearly, especially

when performed with the addition of contrast, it remains insensitive to early

degenerative changes (Malfair & Beall, 2007). Computerised Tomography also has the

ability to generate 3 dimensional images of bony structures. Anular tears may also be

identified on CT when combined with discography, reportedly with greater accuracy

than with MRI. In particular circumferential tears are better visualized with contrast CT

than discogram as they are not continuous with the nucleus pulposus (Kluner et al.,

2006).

2.3.2.4 Diagnostic Ultrasound

There is little support in the literature for the routine use of ultrasonography in imaging

the spine (Tan et al., 2003). It is potentially of some use in assessing paraspinal

structures and measuring cross sectional area of muscle (Hides et al., 2008a) and

enthesitis (D'Agostino et al., 2003).

2.3.2.5 Magnetic Resonance Imaging

There is little disagreement in the literature that MRI and its various modifications have

superseded most other forms of imaging of the spine (Dudler & Balague, 2002). Its

multiplanar ability to accurately image anatomy and its sensitivity to subtle change in

fluid makes it the method of choice from which to assess such changes as IVD

degeneration, herniated NP, bone marrow oedema, inflammation and soft tissue

swelling (Lamminen, 1990; Lamminen et al., 1990; Luoma et al., 2009; Luoma et al.,

2001; Malko et al., 1999; Tan et al., 2003).

MRI has high sensitivity and specificity in detecting disc herniation (Moon et al., 2009),

disc height variations (Boos et al., 1996) and anular tears (Milette et al., 1999).

T2 relaxometry has the important ability to identify free water in the disc which is

known to vary with ageing and degeneration. Changes in total disc volume on MRI

have been used to analyse diurnal changes in fluid content (Malko et al., 1999).

Areas of high intensity on T2 weighted images, while somewhat controversial

(Carragee et al., 2000a; Mitra et al., 2004a; Park et al., 2007; Rankine, 2004), have been

correlated with anular tears and concordant pain (Aprill & Bogduk, 1992; Lam et al.,

2000; Lim et al., 2005). These studies employed discography to determine concordance.

One investigation performed a histological examination post operatively and concluded

Page 44: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 2: Review of Literature

Page II-23

that high intensity zones contained vascularised granulation tissue extending into the NP

(Peng et al., 2006a; Peng et al., 2006b).

2.3.3 Imaging the intervertebral disc

The IVD can be directly visualized with CT, MRI and discography. These modalities

can be used in isolation or combination, with or without contrast medium.

CT can identify disc herniation and anular tears. The addition of contrast allows better

identification of anular tears. MRI also clearly depicts anular tears. Its ability to show

subtle hydration changes, inferred from signal intensity, gives accurate information

regarding degeneration staging (Modic & Ross, 2007; Pfirrmann, 2006).

2.3.3.1 Discography

The introduction of contrast medium to the IVD prior to imaging (discography) has

been considered the gold standard in imaging internal disc disruption and anular tears

(Sofka & Pavlov, 2009) and has been reported as more accurate than MRI in detecting

anulus pathology (Osti & Fraser, 1992). Concomitant provocation of concordant

symptoms during discography has been assumed to enhance its clinical utility in

identification of symptomatic discs however, discography remains a poor predictor of

surgical outcomes (Saboeiro, 2009) with questionable diagnostic value (Kluner et al.,

2006).

The ability of provocative discography to accurately identify disc source of pain has

been questioned (Holt, 1968). Morphological changes within the disc did not correlate

well with painful discs (Ito et al., 1998).

Numerous other studies have reported poor positive predictive value (Walsh et al.,

1990) and an unacceptable rate of false positives (Carragee et al., 2000b).

Carragee (2001) found that concordant pain could be reproduced via discography in

patients with a known non spinal symptomatic source; bone graft donor site pain at the

iliac crest was reproduced on discography (Carragee & Alamin, 2001).

Anular disruption evidenced on discography is a weak predictor of future low back pain

(Carragee et al., 2004).

However, Manchikanti (2009) in a more recent systematic review found that, with strict

adherence to protocols, lumbar discography remained a useful tool in evaluation of

chronic lumbar discogenic pain (Manchikanti et al., 2009).

Page 45: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 2: Review of Literature

Page II-24

Discography alone clearly has questionable diagnostic ability, however it can help

resolve discordance between imaging and clinical findings (Kluner et al., 2006).

Judicious use is recommended as a 10 year matched cohort study by Carragee et al

(2009) linked discography with accelerated rates of degeneration, disc herniation and

reduced disc signal on MRI.

2.3.4 Imaging the nucleus pulposus (NP)

Imaging the NP allows inferences to be made as to physiological, morphological and

putative positional changes of the NP within the IVD.

Apart from discography which, along with anular defects, can highlight the NP, MRI is

the only imaging modality that confers such information to the examiner (Haughton,

2004).

Signal strength from T2 weighted images infers the degree of hydration and, by

extension, potential degenerative change and reduction in proteoglycan content

(Haughton, 2006).

Few studies report morphological or behavioural changes specific to the NP, rather the

majority focus on anular disruption as indicated by failure of NP containment.

Several studies have examined putative NP positional change following changes in

sagittal plane position, using a variety of measurement methods based on T2 weighted

sagittal images (Alexander et al., 2007; Beattie et al., 1994; Brault et al., 1997;

Edmondston et al., 2000; Fennell et al., 1996).

Three dimensional modeling of NP deformation in scoliosis using image processing

software has also been reported (Périé et al., 2001) and correlated with the degree of

deformity (Périé et al., 2003). To date this is the only examination of NP deformation in

planes other than sagittal.

2.3.4.1 Diffusion weighted MRI

Diffusion weighted MRI was originally developed as a tool for early identification of

cerebral ischaemic lesions (Fisher et al., 1992). It uses T2 weighted images to measure

the relative amount of water diffusion (Haughton, 2006). More recently it has been used

to measure water diffusion within and across selected tissues including the IVD (Kealey

et al., 2005; Kerttula et al., 2000).

This technique has been subsequently reported as a reliable method to measure fluid

diffusion in the NP following physical therapy intervention with sagittal plane exercise

Page 46: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 2: Review of Literature

Page II-25

and positioning (Beattie et al., 2010; Beattie et al., 2008). To date this method has not

been tested for sensitivity to differential hydration patterns within the NP.

2.3.5 Quantification of spinal motion and pathology

2.3.5.1 Herniated nucleus pulposus (HNP)

There is much literature describing herniated nucleus pulposus (Kim et al., 2009; Moore

et al., 1996; Parisien & Ball, 1998; Scannell & McGill, 2009) and its natural history to

resorb over time (Atlas et al., 2005; Autio et al., 2006; Benoist, 2002; Cribb et al., 2007;

Kobayashi et al., 2003; Singer et al., 2004). Quantification of the HNP is typically via

linear measurement of the herniated portion (Cribb et al., 2007; Parent et al., 2006a),

linear measurement of the thecal sac or cross sectional area of the thecal sac. These

methods are all considered reliable and linear thecal sac dimensions are reported to

correlate well with cross sectional area (Pneumaticos et al., 2000).

2.3.5.2 Fat infiltration into paraspinal musculature

It has been noted that morphological and histochemical changes occur in muscle

following injury or disease and present as fat infiltration (Yoshihara et al., 2001; Zhao

et al., 2000). This phenomenon has also been reported in association with a variety of

spinal conditions including whiplash associated disorders (Elliott et al., 2006; Elliott et

al., 2008; Elliott et al., 2005) and Duchenne Muscular Dystrophy (Kjaer et al., 2007;

Mengiardi et al., 2006). Fat inflitration has been measured in various ways including

calculation of a muscle/fat index from T1 MRI (Cagnie et al., 2009) and digital image

analysis (Lee et al., 2008). Elliot described a reliable method of comparison by image

analysis of isolated pixel intensities in both muscle and fat from which a percentage of

each can be derived in a select muscle sample (Elliott et al., 2005). A limitation of these

cross sectional studies is their inability to predict changes over time.

2.3.5.3 Muscle cross sectional area

Cross sectional area of muscle has been used to quantify trophic changes. Numerous

studies have employed this measure in analysis of trunk and peripheral muscle injury

using image analysis software (Barker et al., 2004; Herlidou et al., 1999; Hides et al.,

2008b; Kader et al., 2000; Kang et al., 2007; Kjaer et al., 1173; Messineo et al., 1998;

Phoenix et al., 1996). While both ultrasound (Hides et al., 1996) and T1 weighted

magnetic resonance images (Hides et al., 2007) have been used, the majority have

Page 47: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 2: Review of Literature

Page II-26

preferred MRI. Ultrasound based analysis has been reported comparable to MRI

analysis with adherence to strict protocols (Khoury et al., 2008; Stokes et al., 2005)

however clearer visualization of tissue planes on MRI would generally confer greater

accuracy.

2.3.5.4 Measuring segmental axial rotation in the lumbar spine

The first in vivo measurements were reported following insertion of Steinman pins into

the lumbar spinous processes of volunteer subjects (Gregersen & Lucas, 1967).

Subsequent studies have employed techniques such as stereoradiography (Pearcy &

Hindle, 1991a; Pearcy et al., 1984; Pearcy & Tibrewal, 1984) computerized MRI

analysis (Haughton et al., 2002) or CT (Blankenbaker et al., 2006; Singer et al., 2001;

Singer et al., 1989).

Segmental rotation has been measured in idiopathic scoliosis with three dimensional

MRI analysis (Birchall et al., 2005; Birchall et al., 1997) and multiplanar reconstruction

(Liljenqvist et al., 2002). Typically these methods all involve mathematical calculation

of axial plane motion using specific image points or anatomical landmarks on the

adjacent segment. Segmental axial rotation measurement using a variety of techniques

has been prone to observer error (Vrtovec et al., 2009).

Vrtovec has summarized the literature relevant to both two and three dimensional

analysis of segmental rotation (Vrtovec et al., 2010). However, this review

predominantly cites literature relative to scoliosis and neglects earlier two dimensional

in vivo studies (see section 2.1.2.1) or those that relate axial rotation range to

degenerative change (see section 2.2.1.3). These contributions have used a variety of

measurement techniques including stereoradiography (Pearcy & Tibrewal, 1984), twist

CT scans (Singer et al., 2001) and Steinmann pins plus either a protractor (Gunzburg et

al., 1991) or Fastrak motion analysis (Steffen et al., 1997).

2.4 Summary

This chapter has reviewed the literature relevant to the anatomy, physiological

mechanisms, biomechanics and pathology of the lumbar intervertebral disc. The

emphasis has been on aspects of those topics pertinent to torsion, consistent with the

thesis focus on mechanistic studies rather than broader epidemiological surveys. Clearly

there are anatomical and functional features that are torsion specific and the literature

Page 48: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 2: Review of Literature

Page II-27

has reported these to an extent. The literature relevant to imaging techniques employed

in investigation of the IVD has been reviewed, with emphasis on those used in the

investigations of this thesis.

This review highlights that there is limited literature examining lumbar rotation

mechanics. Although more recent studies have examined positional effects on the NP

there remains a paucity of data specific to the NP and its response to torsion. An

omission from the literature is the mapping of hydration pattern changes relative to axial

plane position. While reports exist of unidimensional hydration changes relative to

sagittal plane positioning from single pixel width samples, there are none reporting

biplanar changes with axial rotation positional change. Axial and coronal plane motion

are coupled physiologically necessitating measurement of changes in both planes in

order to accurately evaluate the relative contribution of each to observed hydration

change.

A thorough consideration of this question would require age contrasting, as IVD

hydration changes with age. Investigation should also extend to spinal deformity in

scoliosis where both axial and coronal plane deformity occur in tandem.

Another deficit in the literature is a longitudinal study of changes associated with

rotational disc injury. This should include quantification of changes in paraspinal tissues

relative to IVD changes over time.

Page 49: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 2: Review of Literature

Page II-28

References

Adams M, Bogduk N, Burton K, Dolan P. The Biomechanics of Back Pain. London,

Churchill Livingstone, 2002.

Adams M, Bogduk N, Burton K, Dolan P. The Biomechanics of Back Pain, 2 ed.

London, Churchill Livingstone, 2006.

Adams M, Hutton W. The relevance of torsion to the mechanical derangement of the

lumbar spine. Spine 1981a; 6: 241-8.

Adams M, May S, Freeman B, Morrison H, Dolan P. Effects of Backward Bending on

Lumbar Intervertebral Discs: Relevance to Physical Therapy Treatments for

Low Back Pain. Spine 2000; 25(4): 431-8.

Adams M, McNally D, Chinn H, Dolan P. Posture and the compressive strength of the

lumbar spine. Clinical Biomechanics 1994; 9: 5-14.

Adams MA, Hutton WC. The effect of posture on the role of the apophysial joints in

resisting intervertebral compressive forces. Journal of Bone and Joint Surgery

1980; 62: 358-62.

Adams MA, Hutton WC. The relevance of torsion to the mechanical derangement of the

lumbar spine. Spine 1981b; 6(3): 241-8.

Adams MA, Hutton WC. The effect of posture on the fluid content of lumbar

intervertebral discs. Spine 1983a; 8(6): 665-71.

Adams MA, Hutton WC. The mechanical function of the lumbar apophyseal joints.

Spine 1983b; 8(3): 327-30.

Alexander LA, Hancock E, Agouris I, Smith FW, MacSween A. The response of the

nucleus pulposus of the lumbar intervertebral discs to functionally loaded

positions. Spine 2007; 32(14): 1508-12.

Aprill C, Bogduk N. High-intensity zone: a diagnostic sign of painful lumbar disc on

magnetic resonance imaging. Br J Radiol 1992; 65(773): 361-9.

Atlas SJ, Keller RB, Wu YA, Deyo RA, Singer DE. Long-term outcomes of surgical

and nonsurgical management of sciatica secondary to a lumbar disc herniation:

10 year results from the maine lumbar spine study. Spine 2005; 30(8): 927-35.

Autio RA, Karppinen J, Niinimaki J, Ojala R, Kurunlahti M, Haapea M, Vanharanta H,

Tervonen O. Determinants of spontaneous resorption of intervertebral disc

herniations. Spine 2006; 31(11): 1247-52.

Barker KL, Shamley DR, Jackson D. Changes in the cross-sectional area of multifidus

and psoas in patients with unilateral back pain: the relationship to pain and

disability. Spine 2004; 29(22): E515-9.

Beattie PF, Arnot CF, Donley JW, Noda H, Bailey L. The Immediate Reduction in Low

Back Pain Intensity Following Lumbar Joint Mobilization and Prone Press-ups

Is Associated With Increased Diffusion of Water in the L5-S1 Intervertebral

Disc. J Orthop Sports Phys Ther 2010; 40(5): 256-64.

Beattie PF, Brooks W, Rothstein J. Effect of lordosis on the position of the nucleus

pulposus in supine subjects. Spine 1994; 19: 2096-102.

Beattie PF, Morgan PS, Peters D. Diffusion-weighted magnetic resonance imaging of

normal and degenerative lumbar intervertebral discs: a new method to

potentially quantify the physiologic effect of physical therapy intervention. J

Orthop Sports Phys Ther 2008; 38(2): 42-9.

Behensky H, Cole AA, Freeman BJ, Grevitt MP, Mehdian HS, Webb JK. Fixed lumbar

apical vertebral rotation predicts spinal decompensation in Lenke type 3C

adolescent idiopathic scoliosis after selective posterior thoracic correction and

fusion. Eur Spine J 2007; 16(10): 1570-8.

Benoist M. The natural history of lumbar disc herniation and radiculopathy. Joint Bone

Spine 2002; 69(2): 155-60.

Page 50: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 2: Review of Literature

Page II-29

Beuerlein MJ, Raso VJ, Hill DL, Moreau MJ, Mahood JK. Changes in alignment of the

scoliotic spine in response to lateral bending. Spine 2003; 28(7): 693-8.

Birchall D, Hughes D, Gregson B, Williamson B. Demonstration of vertebral and disc

mechanical torsion in adolescent idiopathic scoliosis using three-dimensional

MR imaging. Eur Spine J 2005; 14(2): 123-9.

Birchall D, Hughes DG, Hindle J, Robinson L, Williamson JB. Measurement of

vertebral rotation in adolescent idiopathic scoliosis using three-dimensional

magnetic resonance imaging. Spine 1997; 22(20): 2403-7.

Blankenbaker DG, Haughton VM, Rogers BP, Meyerand ME, Fine JP. Axial rotation of

the lumbar spinal motion segments correlated with concordant pain on

discography: a preliminary study. AJR Am J Roentgenol 2006; 186(3): 795-9.

Boden SD. The use of radiographic imaging studies in the evaluation of patients who

have degenerative disorders of the lumbar spine. J Bone Joint Surg Am 1996;

78(1): 114-24.

Boden SD, Riew KD, Yamaguchi K, Branch TP, Schellinger D, Wiesel SW.

Orientation of the lumbar facet joints: association with degenerative disc

disease. J Bone Joint Surg Am 1996; 78(3): 403-11.

Bogduk N. Clinical Anatomy of the Lumbar Spine and Sacrum, 4 ed. London: Elsevier

Health Sciences, 2005;

Bogduk N, Twomey L. Clinical Anatomy of the Lumbar Spine. Edinburgh: Churchill

Livingstone, 1987;

Bogduk N, Twomey L. Clinical Anatomy of the Lumbar Spine. Edinburgh: Churchill

Livingstone, 1991;

Boos N, Wallin A, Aebi M, Boesch C. A new magnetic resonance imaging analysis

method for the measurement of disc height variations. Spine 1996; 21(5): 563-

70.

Boos N, Weissbach S, Rohrbach H, Weiler C, Spratt KF, Nerlich AG. Classification of

age-related changes in lumbar intervertebral discs: 2002 Volvo Award in basic

science. Spine 2002; 27(23): 2631-44.

Boszczyk B, Boszczyk A, Putz R. Comparative and Functional Anatomy of the

Mammalian Lumbar Spine. The Anatomical Record 2001; (264): 157-68.

Boyle JJ, Singer KP, Milne N. Morphological survey of the cervicothoracic junctional

region. Spine 1996; 21(5): 544-8.

Brault J, Driscoll D, Laakso L, Kappler R, Allin E, Glonek T. Quantification of lumbar

intradiscal deformation during flexion and extension by mathematical analysis

of magnetic resonance imaging pixel intensity profiles. Spine 1997; 22: 2066-

72.

Bullough P. Histology for Pathologists: Lippincott Williams and Wilkins, 2007;

Burnett A, O'Sullivan P, Ankarberg L, Gooding M, Nelis R, Offermann F, Persson J.

Lower lumbar spine axial rotation is reduced in end-range sagittal postures when

compared to a neutral spine posture. Man Ther 2008; 13(4): 300-6.

Burnett AF, Barrett CJ, Marshall RN, Elliott BC, Day RE. Three-dimensional

measurement of lumbar spine kinematics for fast bowlers in cricket. Clin

Biomech (Bristol, Avon) 1998; 13(8): 574-83.

Cagnie B, Barbe T, Vandemaele P, Achten E, Cambier D, Danneels L. MRI analysis of

muscle/fat index of the superficial and deep neck muscles in an asymptomatic

cohort. Eur Spine J 2009.

Carragee E, Alamin T. Discography: a review. Spine 2001; 1: 364-72.

Carragee EJ, Barcohana B, Alamin T, van den Haak E. Prospective controlled study of

the development of lower back pain in previously asymptomatic subjects

undergoing experimental discography. Spine 2004; 29(10): 1112-7.

Page 51: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 2: Review of Literature

Page II-30

Carragee EJ, Don AS, Hurwitz EL, Cuellar JM, Carrino J, Herzog R. 2009 ISSLS Prize

Winner: Does discography cause accelerated progression of degeneration

changes in the lumbar disc: a ten-year matched cohort study. Spine 2009;

34(21): 2338-45.

Carragee EJ, Paragioudakis SJ, Khurana S. 2000 Volvo Award winner in clinical

studies: Lumbar high-intensity zone and discography in subjects without low

back problems. Spine 2000a; 25(23): 2987-92.

Carragee EJ, Tanner CM, Khurana S, Hayward C, Welsh J, Date E, Truong T, Rossi M,

Hagle C. The rates of false-positive lumbar discography in select patients

without low back symptoms. Spine 2000b; 25(11): 1373-80; discussion 81.

Cholewicki J, Crisco J, Oxland T, Yamamoto I, Panjabi M. Effects of posture and

structure on three- dimensional coupled rotations in the lumbar spine. A

biomechanical analysis. Spine 1996; 21: 2421-8.

Cribb GL, Jaffray DC, Cassar-Pullicino VN. Observations on the natural history of

massive lumbar disc herniation. J Bone Joint Surg Br 2007; 89(6): 782-4.

D'Agostino MA, Said-Nahal R, Hacquard-Bouder C, Brasseur JL, Dougados M, Breban

M. Assessment of peripheral enthesitis in the spondylarthropathies by

ultrasonography combined with power Doppler: a cross-sectional study.

Arthritis Rheum 2003; 48(2): 523-33.

DePalma A, Rothman R. The Intervertebral Disc. Philadelphia: W.B. Saunders, 1970;

Drake JD, Callaghan JP. Do flexion/extension postures affect the in vivo passive lumbar

spine response to applied axial twist moments? Clin Biomech (Bristol, Avon)

2008; 23(5): 510-9.

Dudler J, Balague F. What is the rational diagnostic approach to spinal disorders? Best

Pract Res Clin Rheumatol 2002; 16(1): 43-57.

Dvorak J, Panjabi MM, Chang DG, Theiler R, Grob D. Functional radiographic

diagnosis of the lumbar spine. Flexion-extension and lateral bending. Spine

1991; 16(5): 562-71.

Edmondston S, Song S, Bricknell R, Davies P, Fersum K, Humphries P, Wickendon D,

Singer K. MRI evaluation of lumbar spine flexion and extension in

asymptomatic individuals. Manual Therapy 2000; 5: 158-64.

Elliott J, Jull G, Noteboom JT, Darnell R, Galloway G, Gibbon WW. Fatty infiltration

in the cervical extensor muscles in persistent whiplash-associated disorders: a

magnetic resonance imaging analysis. Spine 2006; 31(22): E847-55.

Elliott J, Sterling M, Noteboom JT, Darnell R, Galloway G, Jull G. Fatty infiltrate in the

cervical extensor muscles is not a feature of chronic, insidious-onset neck pain.

Clin Radiol 2008; 63(6): 681-7.

Elliott JM, Galloway GJ, Jull GA, Noteboom JT, Centeno CJ, Gibbon WW. Magnetic

resonance imaging analysis of the upper cervical spine extensor musculature in

an asymptomatic cohort: an index of fat within muscle. Clin Radiol 2005; 60(3):

355-63.

Fagan A, Moore R, Vernon Roberts B, Blumbergs P, Fraser R. ISSLS prize winner: The

innervation of the intervertebral disc: a quantitative analysis. Spine 2003;

28(23): 2570-6.

Farfan H, Sullivan J. The Relation of Facet Orientation to Intervertebral Disc Failure.

The Canadian Journal of Surgery 1967; 10: 179-85.

Farfan HF. Mechanical disorders of the low back. Philadelphia: Lea & Febiger, 1973;

p247

Farfan HF. Form and function of the musculoskeletal system as revealed by

mathematical analysis of the lumbar spine. An essay. Spine 1995; 20(13): 1462-

74.

Page 52: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 2: Review of Literature

Page II-31

Farfan HF, Cossette JW, Robertson GH, Wells RV, Kraus H. The effects of torsion on

the lumbar intervertebral joints: the role of torsion in the production of disc

degeneration. J Bone Joint Surg Am 1970; 52(3): 468-97.

Fayad F, Lefevre-Colau MM, Drape JL, Feydy A, Chemla N, Quintero N, Rannou F,

Poiraudeau S, Fermanian J, Revel M. Reliability of a modified Modic

classification of bone marrow changes in lumbar spine MRI. Joint Bone Spine

2009; 76(3): 286-9.

Fazey P, Song S, Mønsas A, Johansson L, Haukalid T, Price R, Singer K. An MRI

investigation of intervertebral disc deformation in response to torsion. Clinical

Biomechanics 2006; 21: 538-42.

Fennell A, Jones A, Hukins D. Migration of the nucleus pulposus within the

intervertebral disc during flexion and extension of the spine. Spine 1996; 21:

2753- 7.

Feydy A, Pluot E, Guerini H, Drape JL. Role of imaging in spine, hand, and wrist

osteoarthritis. Rheum Dis Clin North Am 2009; 35(3): 605-49.

Fisher M, Sotak CH, Minematsu K, Li L. New magnetic resonance techniques for

evaluating cerebrovascular disease. Ann Neurol 1992; 32(2): 115-22.

Fraser RD, Osti OL, Vernon-Roberts B. Intervertebral disc degeneration. Eur Spine J

1993; 1(4): 205-13.

Freemont AJ, Peacock TE, Goupille P, Hoyland JA, O'Brien J, Jayson MI. Nerve

ingrowth into diseased intervertebral disc in chronic back pain. Lancet 1997;

350(9072): 178-81.

Fujiwara A, An H, Lim TH, Haughton V. Morphologic Changes in the Lumbar

Intervertebral Foramen Due to Flexion-Extension, Lateral Bending, and Axial

Rotation: An In Vitro Anatomic and Biomechanical Study Spine 2001; 26(8):

876-82.

Giles L, Singer K. Clinical Anatomy and Management of Low Back Pain. Oxford:

Butterworth-Heinemann, 1997;

Gregersen G, Lucas D. In vivo study of the axial rotation of the human thoracolumbar

spine. Journal of Bone and Joint Surgery (British volume) 1967; 49: 247-62.

Grogan J, Nowicki BH, Schmidt TA, Haughton VM. Lumbar facet joint tropism does

not accelerate degeneration of the facet joints. AJNR Am J Neuroradiol 1997;

18(7): 1325-9.

Gunzburg R, Hutton W, Fraser R. Axial rotation of the lumbar spine and the effect of

flexion. An in vitro and in vivo biomechanical study. Spine 1991; 16(1): 22-8.

Gunzburg R, Hutton WC, Crane G, Fraser RD. Role of the capsulo-ligamentous

structures in rotation and combined flexion-rotation of the lumbar spine. J Spinal

Disord 1992; 5(1): 1-7.

Hadjipavlou AG, Tzermiadianos MN, Bogduk N, Zindrick MR. The pathophysiology of

disc degeneration: a critical review. J Bone Joint Surg Br 2008; 90(10): 1261-70.

Haefeli M, Kalberer F, Saegesser D, Nerlich AG, Boos N, Paesold G. The course of

macroscopic degeneration in the human lumbar intervertebral disc. Spine 2006;

31(14): 1522-31.

Harrison DE, Harrison DD, Troyanovich SJ. Three-dimensional spinal coupling

mechanics: Part I. A review of the literature. J Manipulative Physiol Ther 1998;

21(2): 101-13.

Haughton V. Medical imaging of intervertebral disc degeneration: current status of

imaging. Spine 2004; 29(23): 2751-6.

Haughton V. Imaging intervertebral disc degeneration. J Bone Joint Surg Am 2006; 88

Suppl 2: 15-20.

Page 53: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 2: Review of Literature

Page II-32

Haughton V, Rogers B, Meyerand M, Resnick D. Measuring the axial rotation of

lumbar vertebrae in vivo with MR imaging. American Journal of

Neuroradiology 2002; 23: 1110-6.

Herlidou S, Rolland Y, Bansard JY, Le Rumeur E, de Certaines JD. Comparison of

automated and visual texture analysis in MRI: characterization of normal and

diseased skeletal muscle. Magn Reson Imaging 1999; 17(9): 1393-7.

Hides JA, Belavy DL, Stanton W, Wilson SJ, Rittweger J, Felsenberg D, Richardson

CA. Magnetic resonance imaging assessment of trunk muscles during prolonged

bed rest. Spine 2007; 32(15): 1687-92.

Hides JA, Gilmorea C, Stanton W, Bohlscheida E. Multifidus size and symmetry among

chronic LBP and healthy asymptomatic subjects. Manual Therapy 2008a; 13:

43-9.

Hides JA, Richardson CA, Jull GA. Multifidus muscle recovery is not automatic after

resolution of acute, first-episode low back pain. Spine 1996; 21(23): 2763-9.

Hides JA, Stanton WR, Freke M, Wilsom S, McMahon S, Richardson CA. MRI study

of the size, symmetry and function of the trunk muscles among elite cricketers

with and without low back pain. British Journal of Sports Medicine 2008b;

42(10): 509-13.

Holt EP, Jr. The question of lumbar discography. J Bone Joint Surg Am 1968; 50(4):

720-6.

Ito M, Incorvaia KM, Yu SF, Fredrickson BE, Yuan HA, Rosenbaum AE. Predictive

signs of discogenic lumbar pain on magnetic resonance imaging with

discography correlation. Spine 1998; 23(11): 1252-8; discussion 9-60.

Jensen TS, Bendix T, Sorensen JS, Manniche C, Korsholm L, Kjaer P. Characteristics

and natural course of vertebral endplate signal (Modic) changes in the Danish

general population. BMC Musculoskelet Disord 2009; 10: 81.

Jensen TS, Karppinen J, Sorensen JS, Niinimaki J, Leboeuf-Yde C. Vertebral endplate

signal changes (Modic change): a systematic literature review of prevalence and

association with non-specific low back pain. Eur Spine J 2008; 17(11): 1407-22.

Kader DF, Wardlaw D, Smith FW. Correlation between the MRI changes in the lumbar

multifidus muscles and leg pain. Clin Radiol 2000; 55(2): 145-9.

Kang CH, Shin MJ, Kim SM, Lee SH, Lee C-S. MRI of paraspinal muscles in lumbar

degenerative kyphosis patients and control patients with chronic low back pain.

Clinical Radiology 2007; 62: 479-86.

Karacan I, Aydin T, Sahin Z, Cidem M, Koyuncu H, Aktas I, Uludag M. Facet angles in

lumbar disc herniation: their relation to anthropometric features. Spine 2004;

29(10): 1132-6.

Kealey SM, Aho T, Delong D, Barboriak DP, Provenzale JM, Eastwood JD.

Assessment of apparent diffusion coefficient in normal and degenerated

intervertebral lumbar disks: initial experience. Radiology 2005; 235(2): 569-74.

Kerttula LI, Jauhiainen JP, Tervonen O, Suramo IJ, Koivula A, Oikarinen JT. Apparent

diffusion coefficient in thoracolumbar intervertebral discs of healthy young

volunteers. J Magn Reson Imaging 2000; 12(2): 255-60.

Keyes D, Compere E. The Normal and pathological physiology of the nucleus pulposus

of the intervertebral disc: an anatomical, clinical, and experimental study. The

Journal of Bone and Joint Surgery 1932; 14: 897-938.

Khoury V, Cardinal E, Brassard P. Atrophy and fatty infiltration of the supraspinatus

muscle: sonography versus MRI. AJR Am J Roentgenol 2008; 190(4): 1105-11.

Kim MS, Park KW, Hwang C, Lee YK, Koo KH, Chang BS, Lee CK, Lee DH.

Recurrence rate of lumbar disc herniation after open discectomy in active young

men. Spine 2009; 34(1): 24-9.

Page 54: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 2: Review of Literature

Page II-33

Kjaer P, Bendix T, Sorensen JS, Korsholm L, Leboeuf-Yde C. Are MRI-defined fat

infiltrations in the multifidus muscles associated with low back pain? BMC Med

2007; 5: 2.

Kjaer P, Leboeuf-Yde C, Korsholm L, Sorensen J, Bendix T. Magnetic resonance

imaging and low back pain in adults: A diagnostic imaging study of 40-year-old

men and women. Spine. 1173; 30(10): 1173-80.

Kluner C, Kivelitz D, Rogalla P, Putzier M, Hamm B, Enzweiler C. Percutaneous

discography: comparison of low-dose CT, fluoroscopy and MRI in the diagnosis

of lumbar disc disruption. Eur Spine J 2006; 15(5): 620-6.

Ko HY, Park BK. Facet tropism in lumbar motion segments and its significance in disc

herniation. Arch Phys Med Rehabil 1997; 78(11): 1211-4.

Kobayashi N, Asamoto S, Doi H, Ikeda Y, Matusmoto K. Spontaneous regression of

herniated cervical disc. Spine J 2003; 3(2): 171-3.

Kouwenhoven JW, Castelein RM. The pathogenesis of adolescent idiopathic scoliosis:

review of the literature. Spine 2008; 33(26): 2898-908.

Krismer M, Haid C, Rabl W. The contribution of anulus fibers to torque resistance.

Spine 1996; 21(22): 2551- 7.

Kuklo TR, Potter BK, Lenke LG. Vertebral rotation and thoracic torsion in adolescent

idiopathic scoliosis: what is the best radiographic correlate? J Spinal Disord

Tech 2005; 18(2): 139-47.

Lam KS, Carlin D, Mulholland RC. Lumbar disc high-intensity zone: the value and

significance of provocative discography in the determination of the discogenic

pain source. Eur Spine J 2000; 9(1): 36-41.

Lamminen AE. Magnetic resonance imaging of primary skeletal muscle diseases:

patterns of distribution and severity of involvement. Br J Radiol 1990; 63(756):

946-50.

Lamminen AE, Tanttu JI, Sepponen RE, Suramo IJ, Pihko H. Magnetic resonance of

diseased skeletal muscle: combined T1 measurement and chemical shift

imaging. Br J Radiol 1990; 63(752): 591-6.

Lee DY, Ahn Y, Lee SH. The influence of facet tropism on herniation of the lumbar

disc in adolescents and adults. J Bone Joint Surg Br 2006; 88(4): 520-3.

Lee JC, Cha JG, Kim Y, Kim YI, Shin BJ. Quantitative analysis of back muscle

degeneration in the patients with the degenerative lumbar flat back using a

digital image analysis: comparison with the normal controls. Spine 2008; 33(3):

318-25.

Lee LJ, Coppieters MW, Hodges PW. Differential activation of the thoracic multifidus

and longissimus thoracis during trunk rotation. Spine 2005; 30(8): 870-6.

Lee SU, Lee JI, Butts K, Carragee E, Fredericson M. Changes in posterior lumbar disk

contour abnormality with flexion-extension movement in subjects with low back

pain and degenerative disk disease. PM&R 2009; 1(6): 541-6.

Legaspi O, Edmond SL. Does the evidence support the existence of lumbar spine

coupled motion? A critical review of the literature. J Orthop Sports Phys Ther

2007; 37(4): 169-78.

Li G, Wang S, Passias P, Xia Q, Wood K. Segmental in vivo vertebral motion during

functional human lumbar spine activities. Eur Spine J 2009; 18(7): 1013-21.

Liljenqvist UR, Allkemper T, Hackenberg L, Link TM, Steinbeck J, Halm HF. Analysis

of vertebral morphology in idiopathic scoliosis with use of magnetic resonance

imaging and multiplanar reconstruction. J Bone Joint Surg Am 2002; 84-A(3):

359-68.

Page 55: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 2: Review of Literature

Page II-34

Lim CH, Jee WH, Son BC, Kim DH, Ha KY, Park CK. Discogenic lumbar pain:

association with MR imaging and CT discography. Eur J Radiol 2005; 54(3):

431-7.

Little JP, de Visser H, Pearcy MJ, Adam CJ. Are coupled rotations in the lumbar spine

largely due to the osseo-ligamentous anatomy?-a modeling study. Comput

Methods Biomech Biomed Engin 2008; 11(1): 95-103.

Lovett R. The mechanism of the normal spine and its relation to scoliosis. Boston

Medical and Surgical Journal 1905; 153: 349-58.

Lundon K, Bolton K. Structure and function of the lumbar intervertebral disk in health,

aging, and pathologic conditions. J Orthop Sports Phys Ther 2001; 31(6): 291-

303; discussion 4-6.

Luoma K, Vehmas T, Gronblad M, Kerttula L, Kaapa E. Relationship of Modic type 1

change with disc degeneration: a prospective MRI study. Skeletal Radiol 2009;

38(3): 237-44.

Luoma K, Vehmas T, Riihimaki H, Raininko R. Disc height and signal intensity of the

nucleus pulposus on magnetic resonance imaging as indicators of lumbar disc

degeneration. Spine 2001; 26(6): 680-6.

MacDonald D, Moseley GL, Hodges PW. Why do some patients keep hurting their

back? Evidence of ongoing back muscle dysfunction during remission from

recurrent back pain. Pain 2009; 142(3): 183-8.

Macintosh JE, Pearcy MJ, Bogduk N. The axial torque of the lumbar back muscles:

torsion strength of the back muscles. Aust N Z J Surg 1993; 63(3): 205-12.

Malfair D, Beall DP. Imaging the degenerative diseases of the lumbar spine. Magn

Reson Imaging Clin N Am 2007; 15(2): 221-38, vi.

Malko JA, Hutton WC, Fajman WA. An in vivo magnetic resonance imaging study of

changes in the volume (and fluid content) of the lumbar intervertebral discs

during a simulated diurnal load cycle. Spine 1999; 24(10): 1015-22.

Manchikanti L, Glaser SE, Wolfer L, Derby R, Cohen SP. Systematic review of lumbar

discography as a diagnostic test for chronic low back pain. Pain Physician 2009;

12(3): 541-59.

Masharawi Y, Kjaer P, Bendix T, Manniche C, Wedderkopp N, Sorensen JS, Peled N,

Jensen TS. The reproducibility of quantitative measurements in lumbar magnetic

resonance imaging of children from the general population. Spine 2008a;

33(19): 2094-100.

Masharawi YM, Kjaer P, Bendix T, Manniche C, May H, Mirovsky Y, Anekshtein Y,

Jensen TS, Hershkovitz I. Lumbar facet and interfacet shape variation during

growth in children from the general population: a three-year follow-up MRI

study. Spine 2009; 34(4): 408-12.

Masharawi YM, Peleg S, Albert HB, Dar G, Steingberg N, Medlej B, Abbas J, Salame

K, Mirovski Y, Peled N, Hershkovitz I. Facet asymmetry in normal vertebral

growth: characterization and etiologic theory of scoliosis. Spine 2008b; 33(8):

898-902.

McKenzie R, May S. Mechanical Diagnosis and Therapy, 2 ed. Waikanae: Spinal

Publications New Zealand Ltd, 2003;

McMillan DW, Garbutt G, Adams MA. Effect of sustained loading on the water content

of intervertebral discs: implications for disc metabolism. Ann Rheum Dis 1996;

55(12): 880-7.

Mengiardi B, Schmid MR, Boos N, Pfirrmann CW, Brunner F, Elfering A, Hodler J. Fat

content of lumbar paraspinal muscles in patients with chronic low back pain and

in asymptomatic volunteers: quantification with MR spectroscopy. Radiology

2006; 240(3): 786-92.

Page 56: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 2: Review of Literature

Page II-35

Messineo D, Cremona A, Trinci M, Francia A, Marini A. MRI in the study of distal

primary myopathopies and of muscular alterations due to peripheral

neuropathies: possible diagnostic capacities of MR equipment with low intensity

field (0.2 T) dedicated to peripheral limbs. Magn Reson Imaging 1998; 16(7):

731-41.

Miles M, Sullivan W. Lateral bending at the lumbar and lumbosacral joints. Anatomical

Record 1961; 135: 387-97.

Milette PC, Fontaine S, Lepanto L, Cardinal E, Breton G. Differentiating lumbar disc

protrusions, disc bulges, and discs with normal contour but abnormal signal

intensity. Magnetic resonance imaging with discographic correlations. Spine

1999; 24(1): 44-53.

Mitra D, Cassar-Pullicino VN, McCall IW. Longitudinal study of high intensity zones

on MR of lumbar intervertebral discs. Clin Radiol 2004a; 59(11): 1002-8.

Mitra D, Cassar-Pullicino VN, McCall IW. Longitudinal study of vertebral type-1 end-

plate changes on MR of the lumbar spine. Eur Radiol 2004b; 14(9): 1574-81.

Modic MT. Modic type 1 and type 2 changes. J Neurosurg Spine 2007; 6(2): 150-1;

discussion 1.

Modic MT, Herfkens RJ. Intervertebral disk: normal age-related changes in MR signal

intensity. Radiology 1990; 177(2): 332-3.

Modic MT, Ross JS. Lumbar degenerative disk disease. Radiology 2007; 245(1): 43-61.

Moon KP, Suh KT, Lee JS. Reliability of MRI findings for Symptomatic

Extraforaminal Disc Herniation in Lumbar Spine. Asian Spine J 2009; 3(1): 16-

20.

Moore KL. Muscles and Ligaments of the back. In: Giles LGF, Singer KP eds, Clinical

Anatomy and Management of Low Back Pain, Oxford: Butterworth-Heinemann,

1997; pp. 156-64.

Moore RJ, Vernon-Roberts B, Fraser RD, Osti OL, Schembri M. The origin and fate of

herniated lumbar intervertebral disc tissue. Spine 1996; 21(18): 2149-55.

Murtagh FR, Paulsen RD, Rechtine GR. The role and incidence of facet tropism in

lumbar spine degenerative disc disease. J Spinal Disord 1991; 4(1): 86-9.

Nachemson A. Lumbar intradiscal pressure. Acta Orthopaedica Scandinavica,

Supplementum 1960; 43: 1-104.

Nerlich AG, Schleicher ED, Boos N. 1997 Volvo Award winner in basic science

studies. Immunohistologic markers for age-related changes of human lumbar

intervertebral discs. Spine 1997; 22(24): 2781-95.

Newton M, Thow M, Somerville D, Henderson I, Waddell G. Trunk strength testing

with iso-machines. Part 2: Experimental evaluation of the Cybex II Back Testing

System in normal subjects and patients with chronic low back pain. Spine 1993;

18(7): 812-24.

Ng JK, Parnianpour M, Richardson CA, Kippers V. Functional roles of abdominal and

back muscles during isometric axial rotation of the trunk. J Orthop Res 2001;

19(3): 463-71.

Noren R, Trafimow J, Andersson GB, Huckman MS. The role of facet joint tropism and

facet angle in disc degeneration. Spine 1991; 16(5): 530-2.

Osti OL, Fraser RD. MRI and discography of annular tears and intervertebral disc

degeneration. A prospective clinical comparison. J Bone Joint Surg Br 1992;

74(3): 431-5.

Osti OL, Vernon-Roberts B, Fraser RD. 1990 Volvo Award in experimental studies.

Anulus tears and intervertebral disc degeneration. An experimental study using

an animal model. Spine 1990; 15(8): 762-7.

Page 57: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 2: Review of Literature

Page II-36

Panjabi M. How does posture affect coupling in the lumbar spine? Spine 1989; 14:

1002-11.

Parent E, Videman T, Battié M. The Effect of Lumbar Flexion and Extension on Disc

Contour Abnormality Measured Quantitatively on Magnetic Resonance

Imaging. Spine 2006a; 31(24): 2836-42.

Parent EC, Videman T, Battie MC. The effect of lumbar flexion and extension on disc

contour abnormality measured quantitatively on magnetic resonance imaging.

Spine 2006b; 31(24): 2836-42.

Parisien RC, Ball PA. William Jason Mixter (1880-1958). Ushering in the "dynasty of

the disc". Spine 1998; 23(21): 2363-6.

Park JB, Chang H, Kim KW, Park SJ. Facet tropism: a comparison between far lateral

and posterolateral lumbar disc herniations. Spine 2001; 26(6): 677-9.

Park KW, Song KS, Chung JY, Choi JM, Lee JH, Lee CK, Chang BS. High-Intensity

Zone on L-spine MRI: Clinical Relevance and Association with Trauma History.

Asian Spine J 2007; 1(1): 38-42.

Pearcy M, Hindle R. Axial rotation of lumbar intervertebral joints in forward flexion.

Proc Inst Mech Eng [H] 1991a; 205(4): 205-9.

Pearcy M, Portek I, Shepherd J. Three-dimensional x-ray analysis of normal movement

in the lumbar spine. Spine 1984; 9(3): 294-7.

Pearcy M, Tibrewal S. Axial rotation and lateral bending in the normal lumbar spine

measured by three-dimensional radiography. Spine 1984; 9: 582-87.

Pearcy MJ. Twisting mobility of the human back in flexed postures. Spine 1993; 18(1):

114-9.

Pearcy MJ, Hindle RJ. Axial rotation of lumbar intervertebral joints in forward flexion.

Proc Inst Mech Eng [H] 1991b; 205(4): 205-9.

Peng B, Hou S, Wu W, Zhang C, Yang Y. The pathogenesis and clinical significance of

a high-intensity zone (HIZ) of lumbar intervertebral disc on MR imaging in the

patient with discogenic low back pain. Eur Spine J 2006a; 15(5): 583-7.

Peng BMDP, Hao JMD, Hou SMD, Wu WMD, Jiang DMDP, Fu XP, Yang YMD.

Possible Pathogenesis of Painful Intervertebral Disc Degeneration. Spine 2006b;

31(5): 560-6.

Périé D, Curnier D, de Gauzy JS. Correlation between nucleus zone migration within

scoliotic intervertebral discs and mechanical properties distribution within

scoliotic vertebrae. Magn Reson Imaging 2003; 21(9): 949-53.

Périé D, Sales De Gauzy J, Curnier D, Hobatho M. Intervertebral disc modeling using a

MRI method : migration of the nucleus zone within scoliotic intervertebral discs.

Magnetic Resonance Imaging 2001; 19(9): 1245-8.

Peterson CK, Gatterman B, Carter JC, Humphreys BK, Weibel A. Inter- and

intraexaminer reliability in identifying and classifying degenerative marrow

(Modic) changes on lumbar spine magnetic resonance scans. J Manipulative

Physiol Ther 2007a; 30(2): 85-90.

Peterson CK, Humphreys BK, Pringle TC. Prevalence of modic degenerative marrow

changes in the cervical spine. J Manipulative Physiol Ther 2007b; 30(1): 5-10.

Pfirrmann CC. Effect of aging and degeneration on disc volume and shape: A

quantitative study in asymptomatic volunteers. Journal of Orthopaedic Research

2006; 24(5): 1086-94.

Phoenix J, Betal D, Roberts N, Helliwell TR, Edwards RH. Objective quantification of

muscle and fat in human dystrophic muscle by magnetic resonance image

analysis. Muscle Nerve 1996; 19(3): 302-10.

Page 58: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 2: Review of Literature

Page II-37

Pneumaticos SG, Hipp JA, Esses SI. Sensitivity and specificity of dural sac and

herniated disc dimensions in patients with low back-related leg pain. J Magn

Reson Imaging 2000; 12(3): 439-43.

Rahme R, Moussa R. The modic vertebral endplate and marrow changes: pathologic

significance and relation to low back pain and segmental instability of the

lumbar spine. AJNR Am J Neuroradiol 2008; 29(5): 838-42.

Rajasekaran S, Vidyadhara S, Subbiah M, Kamath V, Karunanithi R, Shetty AP,

Venkateswaran K, Babu M, Meenakshi J. ISSLS prize winner: A study of

effects of in vivo mechanical forces on human lumbar discs with scoliotic disc

as a biological model: results from serial postcontrast diffusion studies,

histopathology and biochemical analysis of twenty-one human lumbar scoliotic

discs. Spine 2010; 35(21): 1930-43.

Rankine J. Further doubt is cast on the significance of the high intensity zone. Clinical

Radiology 2004; 59(11): 1000-1.

Reamy BV, Slakey JB. Adolescent idiopathic scoliosis: review and current concepts.

Am Fam Physician 2001; 64(1): 111-6.

Reichmann S. Motion of the lumbar articular processes in flexion-extension and lateral

flexions of the spine. Acta Morphol Neerl Scand 1971a; 8(4): 261-72.

Reichmann S. The postnatal development of form and orientation of the lumbar

intervertebral joint surfaces. Z Anat Entwicklungsgesch 1971b; 133(1): 102-23.

Richardson CA, Snijders CJ, Hides JA, Damen L, Pas MS, Storm J. The relation

between the transversus abdominis muscles, sacroiliac joint mechanics, and low

back pain. Spine 2002; 27(4): 399-405.

Roberts S, Urban JP, Evans H, Eisenstein SM. Transport properties of the human

cartilage endplate in relation to its composition and calcification. Spine 1996;

21(4): 415-20.

Rohlmann A, Zander T, Schmidt H, Wilke HJ, Bergmann G. Analysis of the influence

of disc degeneration on the mechanical behaviour of a lumbar motion segment

using the finite element method. J Biomech 2006; 39(13): 2484-90.

Rousseau MA, Laporte S, Chavary-Bernier E, Lazennec JY, Skalli W. Reproducibility

of measuring the shape and three-dimensional position of cervical vertebrae in

upright position using the EOS stereoradiography system. Spine 2007; 32(23):

2569-72.

Russell P, Pearcy MJ, Unsworth A. Measurement of the range and coupled movements

observed in the lumbar spine. Br J Rheumatol 1993; 32(6): 490-7.

Saboeiro GR. Lumbar discography. Radiol Clin North Am 2009; 47(3): 421-33.

Sato KMDD, Kikuchi SMDD, Yonezawa TMD. In Vivo Intradiscal Pressure

Measurement in Healthy Individuals and in Patients With Ongoing Back

Problems. Spine 1999; 24(23): 2468-74.

Scannell JP, McGill SM. Disc prolapse: evidence of reversal with repeated extension.

Spine 2009; 34(4): 344-50.

Schmorl G, Junghanns H. The Human Spine in Health and Disease, 1st American ed.

New York: Grune and Stratton, 1959;

Schollum ML, Robertson PA, Broom ND. ISSLS prize winner: microstructure and

mechanical disruption of the lumbar disc annulus: part I: a microscopic

investigation of the translamellar bridging network. Spine 2008; 33(25): 2702-

10.

Schollum ML, Robertson PA, Broom ND. A microstructural investigation of

intervertebral disc lamellar connectivity: detailed analysis of the translamellar

bridges. J Anat 2009; 214(6): 805-16.

Page 59: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 2: Review of Literature

Page II-38

Scholten P, Veldhuizen A. The influence of spine geometry on the coupling between

lateral bending and axial rotation. Engineering in Medicine 1985; 14: 167-71.

Shirazi-Adl A. Finite element evaluation of contact loads on facets of a L2-L3 lumbar

segment in complex loads. Spine 1991; 16: 533-41.

Singer K, Boyle J, Fazey P. Comparative anatomy of the zygapophysial joints, Grieve’s

Modern Manual Therapy, Edinburgh: Churchill Livingstone, 2004.

Singer K, Svansson G, Day R, Breidahl W, Horrex A. The utility of diagnosing lumbar

rotational instability from twist CT scans. Journal of Musculoskeletal Research

2001; 5: 45-51.

Singer KP, Day RE, Breidahl PD. In vivo axial rotation at the thoracolumbar junction:

an investigation using low dose CT in healthy male volunteers. Clinical

Biomechanics 1989; 4: 145-50.

Singer KP, Horrex A, Day RE, Breidahl PD. Diagnostic value of rotation CT scans for

determining lumbar segmental instability. , 23rd Annual Scientific Meeting of

ISSLS, Burlington, USA, 1996.

Sofka CM, Pavlov H. The history of clinical musculoskeletal radiology. Radiol Clin

North Am 2009; 47(3): 349-56.

Steffen T, Rubin RK, Baramki HG, Antoniou J, Marchesi D, Aebi M. A new technique

for measuring lumbar segmental motion in vivo. Method, accuracy, and

preliminary results. Spine 1997; 22(2): 156-66.

Stokes IA. Surface strain on human intervertebral discs. J Orthop Res 1987; 5(3): 348-

55.

Stokes IAF. Mechanical function of the facet joints in the lumbar spine. Clinical

Biomechanics 1988; 3: 101-5.

Stokes M, Rankin G, Newham DJ. Ultrasound imaging of lumbar multifidus muscle:

normal reference ranges for measurements and practical guidance on the

technique. Man Ther 2005; 10(2): 116-26.

Tan AL, Wakefield RJ, Conaghan PG, Emery P, McGonagle D. Imaging of the

musculoskeletal system: magnetic resonance imaging, ultrasonography and

computed tomography. Best Pract Res Clin Rheumatol 2003; 17(3): 513-28.

Twomey L, Taylor J. Age changes in lumbar intervertebral discs. Acta Orthop Scand

1985; 56(6): 496-9.

Vanharanta H, Floyd T, Ohnmeiss DD, Hochschuler SH, Guyer RD. The relationship of

facet tropism to degenerative disc disease. Spine 1993; 18(8): 1000-5.

Veres SP, Robertson PA, Broom ND. The influence of torsion on disc herniation when

combined with flexion. Eur Spine J 2010a; 19(9): 1468-78.

Veres SP, Robertson PA, Broom ND. ISSLS prize winner: How loading rate influences

disc failure mechanics: a microstructural assessment of internal disruption.

Spine 2010b; 35(21): 1897-908.

Vicenzino G, Twomey L. Sideflexion and induced lumbar spine conjunct rotation and

its influencing factors. Australian Journal of Physiotherapy 1993; 39: 299-306.

Vital JM, Gille O, Pointillart V, Pedram M, Bacon P, Razanabola F, Schaelderle C,

Azzouz S. Course of Modic 1 six months after lumbar posterior osteosynthesis.

Spine 2003; 28(7): 715-20; discussion 21.

Vrtovec T, Pernus F, Likar B. A review of methods for quantitative evaluation of axial

vertebral rotation. Eur Spine J 2009.

Vrtovec T, Vengust R, Likar B, Pernus F. Analysis of four manual and a computerized

method for measuring axial vertebral rotation in computed tomography images.

Spine 2010; 35(12): E535-41.

Page 60: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 2: Review of Literature

Page II-39

Wachowski MM, Mansour M, Lee C, Ackenhausen A, Spiering S, Fanghanel J,

Dumont C, Kubein-Meesenburg D, Nagerl H. How do spinal segments move? J

Biomech 2009; 42(14): 2286-93.

Walsh TR, Weinstein JN, Spratt KF, Lehmann TR, Aprill C, Sayre H. Lumbar

discography in normal subjects. A controlled, prospective study. J Bone Joint

Surg Am 1990; 72(7): 1081-8.

White A, Panjabi M. Clinical Biomechanics of the Spine, 2 ed. Philadelphia: Lippincott,

1990;

Wilke HJ, Neef P, Caimi M, Hoogland T, Claes LE. New in vivo measurements of

pressures in the intervertebral disc in daily life. Spine 1999; 24(8): 755-62.

Wright N. Imaging in scoliosis. Arch Dis Child 2000; 82(1): 38-40.

Xia Q, Wang S, Passias PG, Kozanek M, Li G, Grottkau BE, Wood KB. In vivo range

of motion of the lumbar spinous processes. Eur Spine J 2009; 18(9): 1355-62.

Yahia LH, Audet J, Drouin G. Rheological properties of the human lumbar spine

ligaments. J Biomed Eng 1991; 13(5): 399-406.

Yamamoto I, Panjabi MM, Crisco T, Oxland T. Three-dimensional movements of the

whole lumbar spine and lumbosacral joint. Spine 1989; 14(11): 1256-60.

Yang KH, King AI. Mechanism of facet load transmission as a hypothesis for low-back

pain. Spine 1984; 9(6): 557-65.

Yantzer BK, Freeman TB, Lee WE, 3rd, Nichols T, Inamasu J, Guiot B, Johnson WM.

Torsion-induced pressure distribution changes in human intervertebral discs: an

in vitro study. Spine 2007; 32(8): 881-4.

Yoshihara K, Shirai Y, Nakayama Y, Uesaka S. Histochemical changes in the

multifidus muscle in patients with lumbar intervertebral disc herniation. Spine

2001; 26(6): 622-6.

Zhang YH, Zhao CQ, Jiang LS, Chen XD, Dai LY. Modic changes: a systematic review

of the literature. Eur Spine J 2008; 17(10): 1289-99.

Zhao WP, Kawaguchi Y, Matsui H, Kanamori M, Kimura T. Histochemistry and

morphology of the multifidus muscle in lumbar disc herniation: comparative

study between diseased and normal sides. Spine 2000; 25(17): 2191-9.

Page 61: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

CHAPTER 3

Page III-1

Methods

3.1 Overview

This chapter describes the methods used in the subsequent chapters and the rationale

underpinning their modification through the development of both the hypotheses and

the thesis. Additionally the influences that informed those changes in method will be

explained.

3.2 Research Design

The studies forming chapters in this thesis use a mix of research designs.

The MRI based studies presented in chapters 5,6,7 and Appendix 4 are observational

cohort studies. Chapter 8 is a retrospective cohort study and chapter 9 a retrospective

longitudinal case study.

3.3 Research Hypotheses

3.3.1 Chapter 4: The ex vivo CT study

The objective of this study was to examine the influence of lumbar zygapophysial joint

anatomy and intervertebral disc pathology on axial torsion response in ex-vivo

ligamentous lumbar spine preparations using 3D motion tracking and computed

tomography (CT). Segmental rotation and zygapophysial joint separation trends were

compared to radiographic evidence of joint orientation and macroscopic evidence of

disc degeneration.

This preliminary study focussed on zygapophysial joint geometry and orientation, and

stage of disc degeneration. Consequently an interest was given to the response within

the internal disc environment, specifically of the lumbar NP, to rotation.

In order to investigate this, a hypothesis was generated that sagittal and axial plane

positions would induce a directionally predictable deformation of the NP. Additionally,

the unknown influence of conjunct coronal plane position was assessed. To investigate

this hypothesis a novel series of studies using MRI was developed.

Page 62: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 3: Methods

Page III-2

3.3.2 The pilot study (Appendix 1)

The aim of this study was to assess a novel method using MRI to track NP deformation

in response to flexion and extension positions, and the combined positions of flexion

with left rotation and extension with left rotation, at L1-2 and L4-5.

3.3.3 The normative cohort MRI study (chapter 5)

This study adopted the method from the pilot study with minor refinement and applied

it to a larger group of young normal subjects to test the hypothesis that NP deformation

resulting from sagittal, axial and conjunct coronal plane segmental positions would

occur predictably towards the convexity. Additionally, any relationship between axial

rotation direction and NP deformation direction would be determined.

3.3.4 The lateral flexion cohort MRI study (chapter 6)

This study sought to assess the effect of coronal plane positioning alone on NP

deformation. This tested the hypothesis that the NP would deform predictably towards

the convexity and with a magnitude proportional to the range of segmental lateral

flexion.

3.3.5 The aged cohort MRI study (chapter 7)

With minor refinement of method, older subjects with signs of lumbar disc degeneration

were assessed with MRI to test the hypotheses that greater segment lateral flexion

would induce the largest NP deformation from the neutral position; that more severe

disc degeneration would reduce the extent of NP deformation following axial or coronal

plane positioning and that the NP would deform contralaterally to the direction of

segmental lateral flexion.

3.3.6 The scoliosis cohort MRI study (chapter 8)

Scoliosis is the primary spinal condition that includes deformity in both axial and

coronal planes. A retrospective observational cohort study was undertaken to test the

hypothesis that in lumbar compensatory scoliotic curves, NP deformation magnitude at

the apex of the curve would be associated with the extent of intersegmental lateral

flexion range.

Page 63: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 3: Methods

Page III-3

3.3.7 The IVD herniation longitudinal case study (chapter 9)

This 12 year retrospective longitudinal single case study followed the natural history of

a rotation injury to the IVD by serial assessment of herniation size, paravertebral muscle

cross sectional area and degree of fat infiltration. It tested the hypothesis that restoration

in paravertabral muscle size and composition occur with normal activity after 12 years.

3.4 Subject Recruitment

3.4.1 Normative and aged cohort studies

Subjects for the MRI studies reported in chapters 5,6,7 and Appendix 4 were selected

from community volunteers including post graduate students at The University of

Western Australia. Approval was obtained from an institutional ethics committee

[Royal Perth Hospital EC2003-101] (Appendix 1) and written consent obtained from

the subjects (Appendix 2, 3).

Inclusion criteria were:

a) Age consistent with the defined range for each study

b) No history of significant low back pain requiring intervention over the past year

c) No contraindications to MRI

Exclusion criteria were:

a) Current or previous low back pain requiring intervention in the preceding year

b) Presence of any contraindication to MRI

a. Any ferromagnetic implants

b. Any implanted mechanical device

c. Intraorbital metal fragments

d. Claustrophobia

e. Pregnancy

3.4.2 Scoliosis cohort MRI study

Cases for this retrospective study were selected following an audit of patients presenting

to the scoliosis clinic at Royal Perth Hospital and listed for corrective surgery between

July 2007 and April 2011. Subjects (n=14) were selected from an inclusive list of all

patients of three spinal deformity surgeons (PW, EM and DD) requiring pre-operative

MRI evaluation to exclude occult neurological pathology (n=113).

Inclusion criteria were MRI evidence of:

a) Secondary lumbar curvature

Page 64: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 3: Methods

Page III-4

b) Availability of mid disc axial T2 weighted images through the apical segment of

the lumbar curve

c) Availability of T1 weighted coronal images through the apex of the lumbar

curve

d) Availability of regional coronal lumbar plain radiographs for measurement of

lumbar Cobb angles

Exclusion criteria were

a) no secondary lumbar curvature

b) incomplete image sequences

3.4.3 IVD herniation longitudinal case study

The subject for this longitudinal single case study was identified, on request, by a

consultant spinal surgeon (PW). Historical imaging was accessed from records in hard

and electronic format. The subject was contacted to seek consent and requested to

present for subsequent MRI assessment by the consultant surgeon for scheduled re

evaluation. Routine written consent for MRI was obtained (Appendix 3).

3.5 Imaging positions and parameters

3.5.1 Ex vivo CT study

Three post mortem human thoracolumbar spines were obtained. Each was positioned in

a purpose built torsion apparatus. A 3Space® FastrakTM

(Polhemus, Vermont, USA)

electromagnetic motion tracking device was used to measure the segmental

displacements occurring in the specimens via sensors attached to the vertebral bodies.

Following a period of pre loading, rotation to right and left was induced in various

sagittal plane positions. The protocol was repeated within a CT imager (Siemans:

Tomoscan, Berlin, Germany) and images obtained in each position.

3.5.2 The pilot and normative cohort MRI studies

Positioning and scanning parameters were identical for both studies. Each subject was

initially positioned supine on the gantry of 1.5T MR imager (Siemens, Berlin,

Germany). A cylindrical roll of towel was placed under the lordosis to extend the

lumbar spine. T1 weighted localizer sagittal and coronal images (TR/TE [24/6], field of

view 400mm, 512x512 matrix) and T2 weighted axial images (TR/TE [5160/102], field

of view 210mm, 384x384 matrix) were acquired with a fast spin echo sequence, slice

Page 65: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 3: Methods

Page III-5

width 4mm. Target segments were L1-2 and L4-5. The subject was then repositioned

into extension plus left trunk rotation by the placement of a dense foam wedge cushion

under the left hemipelvis and image sequences repeated.

Lumbar spine flexion positioning prior to image acquisition was achieved by placement

of wedge cushioning under the sacrum and thorax with pillows to support the flexed

cervical spine and knees. Left trunk rotation in flexion was induced by the placement of

a dense foam wedge under the left hemipelvis in the flexed position.

Figure 3.1: Subject positioning on the MRI gantry into lumbar extension (A) and

lumbar flexion (B). [Image reproduced with permission from Clinical Biomechanics

2006, 21 (538-542)].

This investigations were preliminary, then exploratory. Selection of unilateral trunk

rotation reflected an attempt to minimise cost and time within the magnet, and the

potential discomfort associated with sustained positioning within the MRI. The choice

of left over right trunk rotation was arbitrary. The same method was adopted for

consistency, with respect to subjects’ trunk rotation direction across the studies

described in chapters 5, 7 and Appendix 4.

A

B

Page 66: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 3: Methods

Page III-6

3.5.3 The lateral flexion cohort MRI study

As preliminary results indicated that conjunct lateral flexion induced more directionally

predictable NP deformation, a study with specific primary positioning into lateral

flexion was conducted.

Scanning was extended to include all lumbar segments and intervening IVDs.

Each subject was initially positioned supine on the gantry of a 0.2T horizontally open

MRI unit (AIRIS mate, Hitachi Inc., Sopporo, Japan). The gantry was inserted into the

magnet and a series of T1 and T2 weighted images acquired in both the supine neutral

and laterally flexed position.

The neutral axial T2 weighted images were acquired through the mid disc region from

L1-2 to L5-S1 with a fast spin echo sequence (3120/120 [TR/TE], FOV 260) 8mm slice

thickness and an acquisition time of 6:52 min.

The pelvis was then stabilised with a strap to prevent rotation and the subject was

positioned into left side bending with one assistant manually holding the legs at the

level of the knees to prevent lateral movement. The subject was then asked to actively

laterally flex to the limit of their range. A second assistant applied overpressure via the

shoulders to minimise trunk rotation and to achieve a limit of passive lateral flexion

range, which was maintained passively by the assistants during imaging. Mid disc

image sequences at all levels were repeated using the same parameters.

Additionally, axial T1 weighted images were taken through the bony vertebra of L1 to

S1 using a fast spin echo sequence (385/24.5 [TR/TE], FOV 300) slice thickness 6mm,

acquisition time 5:45 min and coronal T1 images (285/24.5 [TR/TE], FOV 300) 6mm

thickness, 1:34 min to evaluate segmental rotation and lateral flexion respectively.

3.5.4 The aged cohort MRI study

The normative and lateral flexion studies helped identify the issue of coronal slice angle

influence on segmental lateral flexion measurements. In the rotated position, coronal

slices, used to evaluate intersegmental lateral flexion range and direction, may partially

capture regional sagittal curve (Figure 3.2). Coronal slices orthogonal to the axial plane

position for each candidate level were therefore acquired.

Subject positioning was limited to neutral and left trunk rotation to eliminate potential

influence of biplanar positioning on NP deformation direction and range.

Page 67: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 3: Methods

Page III-7

Subjects were positioned on the gantry of a 1.5T MRI unit (Siemens, Berlin, Germany)

in the supine and left rotated positions. A series of T2 weighted axial and T1 coronal

images were acquired.

Figure 3.2: Coronal image slices parallel to the MRI gantry (A,p) in a rotated lumbar

spine may be influenced by sagittal curvature (B). Image slice angle orthogonal to the

rotated segment position (A,o) captures coronal plane positional change.

Axial T2 weighted neutral images were obtained through the mid disc region from L1 –

2 to L5 – S1 using a fast spin echo sequence (TR/TE [3020/102.0], field of view

20.9x16.7cm, 306x384 matrix, 4mm slice thickness).

Coronal T1 weighted images were also obtained at each candidate level with a fast spin

echo sequence (TR/TE [619.0/11.0], field of view 30x30cm, 448x448 matrix 4mm slice

thickness). The coronal slices were oriented orthogonal to the axial position for each

imaged level.

Following acquisition in the neutral position the subjects were repositioned into left

trunk rotation by the placement of a dense foam cushion wedge under the left

hemipelvis and image sequences repeated.

A B

p

o

Page 68: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 3: Methods

Page III-8

3.5.5 The retrospective studies: The scoliosis cohort and longitudinal case studies

Subjects for these studies (described in chapters 8 and 9) had undergone routine

imaging with standard T1 coronal and T2 weighted axial sequencing for MRI in neutral

supine positioning. Additionally, erect P-A radiographs were obtained for all subjects in

the scoliosis study (chapter 8).

3.6 Image analysis

3.6.1 The Ex vivo CT study

CT films obtained were video-digitised, scaled and analysed for zygapophysial joint

angles and separation using image analysis software from the National Institute of

Health, Bethesda, USA (NIH Image, 1.58). Degree of disc degeneration was

subsequently assessed directly from mid-axial slices cut from each disc.

Following all motion studies the medial and lateral margins of the superior articular

facets were marked to determine the joint space length. From the mid point of this line,

2/3 of the joint space was divided into regions. The separation of the joint for each

region was measured and the average separation of the articular surfaces calculated.

3.6.2 The MRI studies of NP deformation and rotation

Image analysis in all MRI studies, with the exception of that in chapter 9, was

undertaken with Image-J software (NIH, Bethesda, USA). Parameters analysed

included: pixel intensity profiles, segmental lateral flexion and axial rotation angles.

3.6.2.1 Pixel profiles of the intervertebral disc to assess hydration

The pilot study (Appendix 1) tracked movement of the peak pixel point which was

assumed to represent direction and magnitude of fluid shift within the IVD. This

method had been used by other authors (Alexander et al., 2007; Brault et al., 1997;

Edmondston et al., 2000); all taking single line samples across sagittal T2 weighted

images. Pixel sampling in the pilot study was derived from mid disc T2 weighted axial

images across which 3 equidistant lines were placed from right to left and anterior to

posterior. Raw pixel intensity data from these lines were normalised to 100 points,

averaged using a Labview software routine (National Instruments, Austin, USA), then

imported into Excel where the direction and magnitude was derived (Figure 3.3).

Page 69: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 3: Methods

Page III-9

Figure 3.3: Pixel data from equidistant samples lines in A-P and lateral directions

across axial T2 weighted images (A) were normalised to 100 points and averaged in a

labview routine (B).

Averaged data from three line samples was considered more representative of hydration

profile than a single line sample. Axial images were considered to capture the broad

distribution of hydration signal better than sagittal images. The basis for using axial

images was the presumption that it would sample more of the disc. All studies used

4mm slice thicknesses from which pixel profiles were derived. Given that lateral and

height dimensions of the disc being, on average, 56mm and 11mm respectively

(Gocmen-Mas et al., 2010), a 4mm sample would represent 7.1% of the disc through the

sagittal plane and 36.4% through the axial plane. With the hydration signal being non

uniform the smaller the sample as a percentage the less representative it would be of the

general trend.

The only exception to this method was the study in the lateral flexion cohort study

(chapter 6) where 6mm slice thickness was used.

Graphic three dimensional representation of hydration signal highlighted the variability

of hydration signal across the disc (Figure 3.4A). Graphs of averaged data also

identified multiple peaks of pixel intensity (Figure 3.4B). The assumption that peak

pixel point movement best represented the total hydration shift was consequently

questioned.

A B

Page 70: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 3: Methods

Page III-10

Figure 3.4: Three dimensional representation of signal strength highlights the

variability of hydration distribution (A). Multiple peaks of maximum hydration points

(arrows) in each sample (B) question the validity of these as accurate representations of

total hydration weighting. Subsequently, area under the curve of each half of the pixel

plot was adopted to derive the percentage weighting.

In order to better capture the weighting of fluid shift subsequent analysis compared total

raw pixel numbers under each half of the averaged data plot to derive a percentage

change in weighting between data from neutral and rotated positions. This was

considered more representative than the movement of a single pixel peak point.

Previous authors used the terminology NP migration creating an concept of movement

of the NP within the anulus. In an intact anulus NP movement is confined and

minimised by the inner capsular fibres. This does not prevent a marked redistribution of

fluid within the confines of the anulus which is captured by the use of all available pixel

numbers under the curve.

Reliability assessment using coefficient of variation for this method on multiple image

samples was consistently <4%.

3.6.2.2 Angle measurements

Angle measurements of segmental rotation, lateral flexion and lumbar Cobb in the

sagittal and coronal planes, were used in the studies from chapters 5 though 8. All

angles were measured within image analysis software Image J.

A B

39 % 61%

Page 71: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 3: Methods

Page III-11

Segmental rotation (θ) was derived from the angle subtended by a line drawn through

mid disc/vertebral body point and the interlaminar point and the image border (Figure

3.5A). This was subtracted from the angle calculated at the subjacent segment to

determine intersegmental range.

Figure 3.5: Segmental rotation angle (θ) was derived by creating an angle between the

the image border and a line through the mid disc and interlaminar points (A).

Intersegmental lateral flexion angles (Ø) were derived from the angle subtended by the

intersection of lines extended from the inferior endplate of one vertebra and the superior

endplate of the subjacent vertebra (B).

Intersegmental lateral flexion (Ø) was measured from coronal T1 weighted images upon

which a line of best fit was placed across endplates adjacent to an IVD (Figure 3.5B).

The angle of intersection was measured as the intersegmental lateral flexion angle.

The lateral flexion cohort study (chapter 6) uses a minor modification to this method as

the lateral flexion angle is measured from the intersection of two lines through the mid

points of lines joining vertebral body corners (cf: chapter 6, Figure 6.2B).

Cobb angles to measure lumbar regional curvature in the sagittal and coronal planes in

the lateral flexion and scoliosis studies respectively, were derived using the method

described by Cobb (1948). Lines were placed along the superior and inferior end plates

of the upper and lower most vertebra in the curve respectively. The angle subtended by

orthogonal lines extending from each was taken as the Cobb angle.

θ

Ø

A B

Page 72: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 3: Methods

Page III-12

3.6.3 The longitudinal case study

This study evaluated lateral and A-P thecal sac dimensions, multifidus cross sectional

area (CSA) and fat infiltration. All data were derived using image analysis software,

Image-J (NIH, Bethesda, USA), calibrated for millmetre (mm) unit measure for all

linear and CSA measurements from the respective image scale markers.

3.6.3.1 Areal and linear measuements

Linear thecal sac dimensions were measured by placing lines across the thecal sac in

both coronal and sagittal planes at points of maximal diameter determined by visual

inspection. Cross sectional area required the outlining of the region of interest (ROI).

Care was taken to exclude intermuscular fat and fascia. Area values in mm were

calculated within Image-J.

3.6.3.2 Fat infiltration of multifidus

The percentage fat infiltration of multifidus was derived from T1 weighted axial images

using a consistent circular region of interest (ROI) identified within muscle tissue of

multifidus, with care to avoid any intermuscular or intramuscular fat. From this region a

histogram of pixel values was produced via Image J which reported maximum and

minimum values (Figure 3.6A).

The same ROI was then positioned into adjacent subcutaneous fat, with care to ensure

the ROI area was unchanged, and a second histogram of pixel values produced (Figure

3.6B).

The mid point between the highest pixel value for muscle and the lowest pixel value for

fat was taken as a cut off point to delineate pixels attributable to fat vs muscle signal.

Finally, the entire area of multifidus was outlined as the ROI as described previously

and a histogram produced (Figure 3.6C).

Raw pixel data from the histogram were imported into Excel where the cut off point

was applied. Raw pixel numbers pertinent to fat and muscle were then derived. The data

for fat was converted to a percentage of the pixel numbers for the entire ROI.

Page 73: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 3: Methods

Page III-13

A

B

C

Figure 3.6 Regions of interest (outlined in yellow) were identified in muscle (A),

subcutaneous fat (B) and multifidus (C). Histograms of pixel data were produced from

each.

3.7 Statistical analysis

Descriptive statistics were used throughout. Reliability of measures was determined by

Coefficient of Variation (CV).

Page 74: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 3: Methods

Page III-14

Angular measurements were all considered to show acceptable reliability with CVs

<3% and NP deformation percentage <4% from repeated measures of representative

images.

Pearson’s correlation coefficient was used to determine associations between variables

where appropriate, in particular that of NP deformation and segmental angular measures

in coronal and axial planes.

For all tests of statistical significance a probability of p<0.05 was taken to represent

meaningful differences.

Page 75: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 3: Methods

Page III-15

References

Alexander LA, Hancock E, Agouris I, Smith FW, MacSween A. The response of the

nucleus pulposus of the lumbar intervertebral discs to functionally loaded

positions. Spine 2007; 32(14): 1508-12.

Brault J, Driscoll D, Laakso L, Kappler R, Allin E, Glonek T. Quantification of lumbar

intradiscal deformation during flexion and extension by mathematical analysis

of magnetic resonance imaging pixel intensity profiles. Spine 1997; 22: 2066-

72.

Cobb J. Outline for the study of scoliosis. American Academy of Orthopaedic Surgeons.

Instructional Course Lectures 1948; 5: 261-75.

Edmondston S, Song S, Bricknell R, Davies P, Fersum K, Humphries P, Wickendon D,

Singer K. MRI evaluation of lumbar spine flexion and extension in

asymptomatic individuals. Manual Therapy 2000; 5: 158-64.

Gocmen-Mas N, Karabekir H, Ertekin T, Edizer M, Canan Y, Duyar I. Evaluation of

Lumbar Vertebral Body and Disc: A Stereological Morphometric Study.

International Journal of Morphology 2010; 28(3): 841-7.

Page 76: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

CHAPTER 4

Page IV-1

The ex vivo CT study

4.1 Summary

Spinal motion assessment provides insight into the mechanical response of the mobile

segments and is important in the assessment of spinal instability. Radiological and

laboratory investigations have been limited by the complexities of recording rotation

motion which arise when the spine is deformed by torsion. Specifically, there have been

comparatively few investigations into the influence of zygapophysial joint and disc

degeneration on segmental axial plane motion in the lumbar spine.

A torsion apparatus was constructed to induce torsional loading in three ligamentous

lumbar spine preparations. Rotation displacements were recorded first with a Fastrak

3D motion tracking device to assess the effect of load increments in: neutral, flexion

and extension positions. Zygapophysial joint morphology was examined using a CT

protocol to relate macroscopic evidence of disc and facet joint degeneration to each

segment’s response to torsion.

Marked individual variation in both stage of disc and facet degeneration and

geometrical configuration of the zygapophysial joints was observed. Axial rotation and

joint separation was greatest for the lower lumbar segments which corresponded with

more coronal joint angles. Slight flexion generally resulted in increased segmental

rotation compared with neutral and extension positions, except in the presence of

marked segmental degeneration. The case with the most advanced disc degeneration

showed the greatest axial rotation and separation responses.

Separation of the zygapophysial joint is a normal response during axial rotation

movements. However, anatomical configuration of the paired zygapophysial joints, and

the stage of degenerative disc disease impacts on segmental mobility.

Page 77: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 4: The Ex vivo CT study

Page IV-2

4.2 Introduction

Factors influencing spinal segmental motion include the anatomical configuration of the

bony elements, compliance of non contractile soft tissue structures including the

intervertebral disc (IVD) and the active stabilizing function of muscles (Figure 4.1).

Spinal segmental instability occurs when the spine is unable to maintain its pattern of

displacement under physiologic load and is considered an important contributor to low

back pain (Mimura et al., 1994; Nachemson, 1985; Panjabi, 1992) and may involve

disease of the intervertebral disc (IVD) and the zygapophysial joints (ZJ), either singly

or in combination. The role of the ZJs in the lumbar spine is considered to be primarily

one of resistance to excessive rotary and shear forces (Farfan et al., 1972).

Figure 4.1: The lumbar functional spinal unit comprises the paired zygapophysial

joints, the intervertebral disc and the related muscles and ligaments (A); transverse

plane rotation occurs close to the posterior anulus ex vivo and anterior to the anulus in

vivo (B). Segmental rotation induces concurrent motion in the coronal and sagittal

planes (C).

Individual anatomical variation results in individualised movement patterns (Dupuis et

al., 1985). Most studies investigating axial rotation with human cadaveric material

report early structural failure at a mean range of over 2° per segment (Adams & Hutton,

1981; Ahmed et al., 1990; Farfan et al., 1970; Gunzburg et al., 1991; Liu et al., 1985;

Markolf, 1972; McFadden & Taylor, 1990; Schultz et al., 1979; Tencer et al., 1982).

During axial rotation the ZJ surfaces contralateral to the motion direction are

compressed while the ipsilateral joint surfaces separate from each other (Pearcy &

Tibrewal, 1984). These are termed ‘compression’ and ‘tension’ facets, respectively. The

axis of rotation migrates towards the compression facet as the range of axial rotation

increases (Wachowski et al., 2009). Additionally, axial rotation is normally coupled

with both coronal and sagittal plane rotations (Panjabi, 1992; Pearcy & Hindle, 1991).

The influence of ZJs is important in evaluation of any motion segment behaviour

A B C

Page 78: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 4: The Ex vivo CT study

Page IV-3

(Grobler et al., 1993). Coronally orientated joints confer less restraint to axial rotation,

(Cyron & Hutton, 1980; Farfan et al., 1972) with Duncan and Ahmed (Duncan &

Ahmed, 1991) noting more oblique orientation and flat geometry of the compression

facet facilitates axial rotation. An increase in axial rotation in the lumbar spine, when

moving from an extended to a flexed position, has also been observed (Duncan &

Ahmed, 1991). However, in vivo and cadaveric studies conducted by Gunzburg et al

contradict these findings; which in part reflects variations between ex vivo and in vivo

designs (Gunzburg et al., 1991). In subsequent investigations by Pearcy & Hindle of

ligamentous lumbar segments tested in the neutral position and then various ranges of

flexion, they confirmed that sub-maximal flexion increases the available axial torsion

range in the lumbar spine (Pearcy & Hindle, 1991).

Segmental instability has been considered an inevitable sequel to the degenerative

process, involving both the IVD and the ZJs, resulting in a temporary increase in motion

due to laxity of the connective tissue restraints (Haughton et al., 2002; Kirkaldy-Willis,

1988). A variable response to axial rotation in degenerated motion segments has been

observed in many studies (Adams & Hutton, 1981; Blankenbaker et al., 2006; Farfan et

al., 1970; Mimura et al., 1994). Segments with degenerated ZJs or IVDs have

demonstrated a larger neutral zone during rotation testing with aberrant motion patterns

at small ranges of rotation (Adams & Hutton, 1981; Farfan et al., 1970; Mimura et al.,

1994). According to Adams & Hutton, degenerated IVDs allow approximately 7° of

rotation per segment before failure, whereas normal segments confer <2° (Adams &

Hutton, 1981). End stage segment disease involving autofusion from osteophytosis is

intended to inhibit motion and finite element modelling confirms reduced axial rotation

range at intervertebral levels with higher grades of degeneration (Rohlmann et al.,

2006).

Visualisation of motion abnormalities in the lumbar segments has proven difficult,

(Pope et al., 1992; Reichmann, 1973) particularly with respect to axial rotation (Vrtovec

et al., 2010). With the advent of computed tomography (CT) and Magnetic Resonance

Imaging, anatomical assessment of the ZJs has improved, including an understanding of

their contribution to motion segment control. Zygapophysial joints have been implicated

in excess axial rotation motion in unstable cadaveric specimens (Yong-Hing et al.,

1976). In an attempt to demonstrate suspected clinical instability, Kirkaldy-Willis

Page 79: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 4: The Ex vivo CT study

Page IV-4

(Kirkaldy-Willis & Hill, 1979) recommended CT scanning in a supine rotated position

(the twist CT test). This demonstrated narrowing of the lateral recess and abnormal

separation in the tension facet (Kirkaldy-Willis & Tchang, 1988). The ‘twist CT’ has

been successfully employed in the cervical spine to examine rotation displacements in

normal and symptomatic populations (Dvorak et al., 1987; Penning & Wilmink, 1987).

Such a test was subsequently proposed by Graf (Graf, 1992) as a diagnostic predictor of

rotational instability in the lumbar spine. Graf considered separation of the lumbar ZJ

surfaces >1.5 mm as a diagnostic threshold for instability, however the basis for this

criteria has not been validated against normal reference ranges. Increased axial rotation

ranges using this test were demonstrated at degenerated segments in patients by

Blankenbaker et al which elicited concordant pain on subsequent discography

(Blankenbaker et al., 2006).

An important question has been to determine the normal and pathological response to

torsion. Using a low dose CT protocol to examine axial rotation in lower thoracic and

upper lumbar segments in normal male subjects, evident separation of the tension ZJs in

asymptomatic subjects was reported, although the actual rotation range per segment was

small (Singer et al., 1989). In a later study (Singer et al., 2001) using twist CT scans of

lower lumbar segments of 79 patients with lumbar spine disease significantly more

separation was shown in coronal compared with sagittal orientated ZJs.

Zygapophysial joint orientation and geometry, as well as degenerative changes,

potentially influence the response to lumbar torsion. The purpose of this study was to

examine the effect of torsion in cadaveric lumbar spine segments, by comparing axial

rotation with ZJ separation, then contrasting this response with macroscopic segment

degeneration of the mobile segments. It was anticipated that the anatomical morphology

of the ZJs coupled with the pathology of the motion segment would be associated with

the extent of separation under torsion load.

4.3 Methods

Thoracolumbar spine specimens obtained at autopsy were stored frozen at -20°C.

Anteroposterior and lateral radiographs were used to exclude any specimens with

evidence of prior surgery, tumour or ankylosis. The three cases of average height and

weight were designated A (male aged 61), B (male aged 85) and C (female aged 80

Page 80: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 4: The Ex vivo CT study

Page IV-5

years). Prior to testing, each case was thawed and cleaned of all muscle tissue leaving

the osteoligamentous spine intact from T12 to the sacrum.

The most superior and inferior vertebral bodies were positioned and fixed into cups

using titanium screws and bone cement, then secured in a custom torsion apparatus

(Figure 4.2A). Due to the lack of sacral fixation available in two cases (B&C), the L4-5

level was not tested in Case B and C. Once positioned into the torsion rig, each case was

orientated in neutral, or in 5° of flexion or extension.

The 3Space FastrakTM

(Polhemus, Vermont, USA) electromagnetic motion tracking

device was used to record the segmental movements in each case. Labview software

(National Instruments, USA) was used to control the Fastrak device and acquire motion

data.

Tracking sensors were attached to the lumbar vertebral bodies using rigid perspex

holders (Figure 4.2B). Case A was tested using torsional strain increments of 5, 10 and

15kg applied via pulleys using free weights. The lever arm of the rotation axis in the

torsion apparatus resulted in torsional loads of: 5Nm, 10Nm and 15Nm, respectively. To

accommodate creep each case was pre-loaded for 2 minutes prior to recording the range

of movement. In the older specimens (B and C), the 15kg load increment was not

applied to minimize risk of tissue failure. The range of right and left rotation was

measured under each load increment with the specimens in a neutral, then flexed

followed by extended positions. For this report only the 10Nm load data are presented.

Following motion measurement with the Fastrak system, each specimen was fitted into

the torsion apparatus, placed into a Perspex water tank, to simulate soft-tissues, and

scanned parallel with the superior vertebral end-plate of each candidate vertebra. A

lateral scout view in each unloaded position was obtained to facilitate alignment of the

CT gantry. The loading protocol used for the CT scanning was the same as for

recording Fastrak data.

Page 81: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 4: The Ex vivo CT study

Page IV-6

Figure 4.2: The torsion apparatus was positioned in situ within a water tank during

testing and scanning (A). To produce axial torsion in the specimen, load was

introduced by weights applied to cords around the proximal torque cup (TC). This cup

was restrained on the apparatus frame to provide fixation of the specimen into either:

neutral, 5° flexion or 5° extension. The Fastrak (F) tracking sensors (S) were attached

to Perspex stem holders which were screwed into the vertebral bodies of the specimen

(B).

The specimen was then removed from the torsion apparatus and segments dissected

transversely through the disc and posterior elements. Disc degeneration was graded

according to criteria described by Nachemson(Nachemson, 1960) (Grade I: normal,

Grade II: moderate degeneration, Grade III: advanced degeneration). The degenerative

status of the ZJs was macroscopically classified into four categories. Grade I: normal

A

B

Page 82: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 4: The Ex vivo CT study

Page IV-7

articular cartilage, Grade II: fine fibrillation, Grade III: coarse fibrillation, and Grade

IV: enurbation of articular cartilage to subchondral bone.

The CT images for every level were video-digitised, scaled and analysed using NIH

Image software (Image J, NIH Bethesda, USA,). For each image the paired ZJ angles

were derived from a median sagittal reference line (Figure 4.3A).

To calculate the separation of the ZJs, each joint was enlarged (x3) with bilinear

interpolation and a threshold established using the gray scale value of cortical bone. The

medial and lateral margins of the superior articular facets were marked to determine the

joint space length. From the mid point of this line, 2/3 of the joint space was divided

into regions. The separation of the joint for each region was measured and the average

separation of the articular surfaces defined (Figure 4.3B).

The image analysis process error was estimated by repeated measurements of one image

and calculating the coefficient of variation (CV). Using cortical bone to establish a

constant image threshold the intra-examiner CV was 1.6% for all measures.

Figure 4.3: From the CT image a sagittal median reference plane was established by

extending a line from the centroid of the vertebral body to the inter-laminar junction of

the posterior elements. A line drawn from the lateral to the medial borders of the

superior articular facet was extended to the medial sagittal reference plane and the

orientation of the zygapophysial joints, in degrees, was established (A). The CT scale

was used to reference the zoomed (x3) and thresholded image; then the midpoint of the

line determining the length of the joint, was used to calculate the physical separation of

the middle 2/3 of the joint space (B).

Page 83: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 4: The Ex vivo CT study

Page IV-8

Pilot studies using the Fastrak system indicated an accuracy of 0.01°, repeatability

coefficient of variation was 0.6%, and the system noise in the laboratory was 0.01°.

Descriptive statistics were used to present trends for rotation responses. The association

between the zygapophysial morphology and separation was assessed with simple linear

regression. A probability of p<0.05 was used as the criterion to reflect a meaningful

association.

4.4 Results

The results for each case are presented in four sections describing I: the ZJ orientation

and degenerative grade of the motion segments, II: the axial-torque response, III: the ZJ

separation in response to torsion and, IV: the influence of sagittal position on axial

rotation and ZJ separation response.

I: Zygapophysial joint orientation and degenerative grading of mobile segments

Case A demonstrated a gradual caudal increase in coronal ZJ alignment, Case B showed

predominantly sagittal orientation, and Case C presented more coronal orientatation.

The ZJ surfaces differed geometrically between cases. Case A had relatively flat joint

surfaces by comparison, Case B demonstrated ‘J’ shaped joints with large restraining

mammillary processes, while Case C demonstrated deep ‘C’ shaped joints. Relative ZJ

symmetry was present at all levels, however as variations of less than 6° are considered

normal, only three segments fulfilled the criteria for asymmetry (Table 4.1).

Figure 4.4 illustrates the macroscopic CT features at the level of the superior end-plate

for each case at the L3-4 level, contrasting: neutral, left and right torsion responses

under a 10Nm load.

Table 4.1: Segmental orientation of the zygapophysial joints as measured from the sagittal

reference plane. Orientation of the right and left joints for each case are reported (data are

in degrees).

Case A Case B Case C

R L R L R L

L1-2 13.6 15.7 7.2 11.1 36.6 33.0

L2-3 31.9 36.8 17.6 11.1 * 31.1 42.6 *

L3-4 37.9 38.9 25.7 30.4 45.8 37.2 *

L4-5 49.1 54.3 – –

(*: denotes zygapophysial joint asymmetry > 6)

Page 84: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 4: The Ex vivo CT study

Page IV-9

Figure 4.4: The rotation sequences for all cases at level L3/4 are presented. The CT

sections were obtained after 10Nm load to the right (I) and to the left (II). The middle

image (N) in all cases represents no load. Note the different anatomical and geometrical

configurations of the posterior joints. The flat joint surfaces of Case A, compared to the

sagittally aligned joints in Case B. In Case C, the ‘C’ shaped geometry of the

zygapophysial joints can be observed, in particular, the excessive separation following

rotation.

Page 85: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 4: The Ex vivo CT study

Page IV-10

The degenerative condition of the ZJs were similar. Apart from three upper lumbar

segments, other levels showed marked fibrillation or enurbation of the articular

cartilage. In general, the articular cartilage of the sagittal component of the joints

demonstrated greater change than the coronal component. Posterior margin osteophytes

were noted on the right side of the ZJ at L3-4 in Case B. The degree of IVD

degeneration was similar for Cases A and B. Large osteophytes were noted laterally on

the right side of the L3-4 in Case A, while at L1-2 in Case B there was calcification in

the outer anulus with anterior osteophytes. All IVD’s for Case C demonstrated marked

degeneration with calcification of the outer anulus. Macroscopic degenerative

classification of the ZJs and IVDs for all motion segments is presented in Table 4.2.

Table 4.2: Macroscopic degenerative changes of the zygapophysial joints and

intervertebral discs.

Case A Case B Case C

Joint

Degen

Disc

Degen

Joint

Degen

Disc

Degen

Joint

Degen

Disc

Degen

R L R L R L

L1-2 II I III III II III II III III L2-3 IV III III IV III III IV III III L3-4 IV III III III IV III IV IV III L4-5 IV IV III

II: Axial torque response

Axial torque data were recorded for each specimen by using the cranial vertebra of each

motion segment as a reference point and subtracting the angle of each subjacent level

(Table 4.3). The mean segmental unilateral axial rotation response for Case A, under 10

Nm, was 1.2° (range 0.28° - 2.66°). For Case B a mean of 2.6° (range 0° - 3.02°). Case

C demonstrated the highest mean of 3.7° (range 1.94 - 5.28°). Segmental rotation angles

were generally greater in the lower than the upper lumbar spines. An example of the

axial torque-rotation response, for the L3-4 segment of each case, under 10Nm load for:

neutral, flexion and extension positions, is presented in Figure 4.5.

Page 86: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 4: The Ex vivo CT study

Page IV-11

Figure 4.5: Graphical presentation of the right and left rotation response in each case at

L3/4 under 10Nm loading.

Table 4.3: Summary of axial plane motion for all cases, in a neutral position. Rotation in

the axial plane was derived from Fastrak and was measured after 10 Nm loading of the

specimens. (Data are in degrees).

Case A Case B Case C

R L R L R L

L1-2 0.36 0.28 0.01 2.21 1.94 2.89

L2-3 0.52 0.54 2.83 3.02 3.58 3.54

L3-4 1.82 2.66 2.98 1.92 5.28 5.22

L4-5 2.20 1.25 – –

III: Imaging of zygapophysial joint separation in response to torsion

Following rotation loading the ZJ space ipsilateral to the movement direction widened.

Under 10Nm loading in the neutral position, the mean joint separation for Cases A & B

was 2.3mm (range 1.8 - 2.9mm) and 2.3mm (range 1.3 - 3.0 mm), respectively. In

contrast the mean separation in Case C was more marked at 3.8mm (range 2.9 -

5.1mm). The left to right separation response, for each level following 10Nm load in the

neutral position, is presented in Table 4.4.

The measured separation was greater for the lower lumbar segments in Cases A and C.

The separation in Case B was similar for all levels except L2-3 where it increased

following right rotation and decreased at L3-4 following left rotation. The ZJ separation

Page 87: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 4: The Ex vivo CT study

Page IV-12

response to 10Nm load of the L3-4 segment in each case is depicted in Figure 4.6

revealed a significant correlation (R2 0.69, p<0.001).

To appreciate the separation response in relation to the torque-rotation loading

increments, all cases were scanned in semi-flexed and extended positions. The ZJ

separation in the tension facets, demonstrated that the majority of the separation

occurred under minimal loading, in neutral, semi-flexion and extension.

Table 4.4: Summary of tension zygapophysial joint separation in millimeters for all

Cases, in a neutral position with 10Nm loading.

Case A Case B Case C

R L R L R L

L1-L2 1.80 2.16 2.39 2.46 2.96 3.81

L2-L3 2.28 1.88 3.00 2.42 3.58 3.60

L3-L4 2.55 2.79 2.22 1.37 3.50 5.06

L4-L5 2.50 2.86 – –

Figure 4.6: The association between the separation response at levels for all cases.

Each case was clustered according to the relative degree of degeneration exhibited, with

Case C showing the widest separation and segmental rotation as a function of the stage

of age-related changes.

Page 88: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 4: The Ex vivo CT study

Page IV-13

IV: Effect of sagittal position on axial rotation and zygapophysial joint separation

response

Segmental flexion achieved slightly more rotation compared with neutral under the

10Nm load (Table 4.5), with a trend to a reduction in mild extension. Similar trends

were observed for ZJ separations of the tension facet which increased in semi-flexion,

and decreased or no change in the semi-extended position.

Table 4.5: Combined left and right segmental rotation responses for L1-2 to L4-5,

recorded by Fastrak 3D system for three cases subjected to a 10Nm torsional

strain.

Case A Case B Case C

Neutral

L1-2 0.6 2.2 4.8

L2-3 1.1 5.8 7.1

L3-4 4.5 4.9 10.5

L4-5 3.5 – –

5 ° Flexion

L1-2 0.7 2.1 6.8

L2-3 1.5 5.5 6.5

L3-4 4.6 3.7 7.3

L4-5 2.6 – –

5° Extension

L1-2 0.6 1.4 3.8

L2-3 1.0 5.0 7.5

L3-4 3.2 4.2 9.5

L4-5 2.3 – –

All data are degrees (°)

4.5 Discussion

This study examined the response to incremental axial rotation loading in three

cadaveric lumbar spines, each representing stages in age-related spine disease of the

IVD and ZJ of their respective motion segments.

As expected, the torsion responses and zygapophysial separation between and within

cases, reflected individual variations in joint morphology and phase of degeneration of

the mobile segment. The ranges of segmental rotation recorded were similar to those

previously reported (Ahmed et al., 1990; Farfan et al., 1970; Gunzburg et al., 1991).

There was a general trend towards increased axial rotation in the more coronally

oriented lower joints (Table 4.3). The more advanced degeneration in Cases B and C

Page 89: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 4: The Ex vivo CT study

Page IV-14

may explain their increased rotation range relative to Case A. The IVDs of these

specimens all showed advanced degeneration which may have contributed to an

increased range of axial rotation. In these three cases, asymmetry of the paired

zygapohysial joints was not marked and did not appear to influence the rotation.

The effects of change in sagittal plane posture on the axial rotation response measured

in the current study support the findings of Pearcy and Hindle (Pearcy & Hindle, 1991).

Segments semi-flexed up to 5° generally showed a slight increase in axial rotation range

compared to the neutral position. This decreased range in full flexion acts to ‘unlock’

the ZJs but putatively increases shear compression of the anteromedial region of the ZJs

and increases tension in the posterolateral anulus. The 5° extension achieved in all cases

resulted in an overall reduction in rotation in all segments, or was equivalent to ranges

produced in the neutral position. This finding is explained by the greater approximation

of the ZJs into extension positions.

There are numerous descriptions in the literature of lumbar ZJ separation in response to

axial rotation. The tension facet was reported by Farfan et al (Farfan et al., 1970) in

some cases to open by 10mm before failure. Liu et al (Liu et al., 1985) measured a

cartilage filled gap of about 1.5mm between ZJ surfaces and suggested the articular

cartilage may be compressed 60% during rotation. Separation in the tension facet is a

normal ZJ response rather than a sequel to injury or part of segmental instability. The

separation response is not only explained by orientation of the joints alone, as their

shape, integrity of the ligamentous capsule and IVD, also influence this response. In

Case C the marked enurbation of articular cartilage contributed to the greater separation

of the tension facets compared to Case A.

All specimens tested demonstrated moderate to advanced degenerative changes to their

functional spinal segments. The condition of the ZJ cartilage was similar for most cases

with Case C also exhibiting the most degenerated discs which may have contributed

more ‘free play’ before firm apposition occurred in the compression facet (Adams &

Hutton, 1981). Greater laxity was noted by Farfan et al (Farfan et al., 1970) during

torsion in segments with degenerated discs and consequently their torque-rotation

curves were initially flatter. Similarly Mimura et al (Mimura et al., 1994) found an

increase in the neutral zone of the axial rotation range in segments with disc

degeneration. The instantaneous axis of rotation (IAR) in degenerated motion segments,

has been demonstrated to lie in the posterior part of the IVD (Farfan, 1973). As the IAR

Page 90: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 4: The Ex vivo CT study

Page IV-15

moves from the vicinity of the ZJ into the disc, more of the rotation constraint is

demanded of the ZJs (Haher et al., 1992). The recent in vivo study by Xia et al (Xia et

al., 2010) of lumbar segment response to transverse plane motion highlighted a marked

discord in IAR position between ex vivo investigations and in vivo studies. In part these

differences are assumed to be due to imposed constraints of the torsion rig compared

with true physiological rotation axes.

The separation response observed in the current case series may be explained by the

advanced IVD degeneration in the material tested along with the sustained nature of the

load regime during the CT sequences.

In Case A, the CT scans were taken under three increments of loading and the

separation measured. Interestingly most of the separation response was detected after

the first increment of loading (5Nm), the subsequent two increments adding little to the

response. This may suggest that the separation of the facets is first a response to

compression of the articular cartilage and secondly a function of the altered neutral

zone.

Axial rotation is normally constrained in the lumbar spine by the anulus of the IVD and

the lateral aspect of the zygapopysial joints, reflected in the typically limited range of

physiological rotation. A limitation of the instrument used to induce torsion in these

cases was the constrained nature of end-fixation which did not allow physiological

coupled motion of an unrestrained spinal segment.

These cases highlight the variable behaviour of the ZJs under axial rotation loads. To

fully understand the ZJ separation response, more elaborate torsion systems are required

utilizing unconstrained tissues which enable more physiological motion patterns to

occur. As zygapophysial separation is influenced by both anatomical and pathological

factors, an improved understanding of their contributions may be gained from studies

examining the torsion response in tissues which reflect the normal through to advanced

stage pathology continuum. Imaging of the response of the IVD, particularly the

nucleus pulposus, to rotation may elucidate the mechanics of this structure and its

response to segmental rotation.

Page 91: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 4: The Ex vivo CT study

Page IV-16

4.6 References

Adams MA, Hutton WC. The relevance of torsion to the mechanical derangement of the

lumbar spine. Spine 1981; 6(3): 241-8.

Ahmed AM, Duncan NA, Burke DL. The effect of facet geometry on the axial torque-

rotation response of lumbar motion segments. Spine 1990; 15(5): 391-401.

Blankenbaker DG, Haughton VM, Rogers BP, Meyerand ME, Fine JP. Axial rotation of

the lumbar spinal motion segments correlated with concordant pain on

discography: a preliminary study. AJR Am J Roentgenol 2006; 186(3): 795-9.

Cyron MB, Hutton WC. Articular tropism and stability of the lumbar spine. Spine 1980;

5: 168-72.

Duncan NA, Ahmed AM. The role of axial rotation in the etiology of unilateral disc

prolapse. An experimental and finite-element analysis. Spine 1991; 16(9): 1089-

98.

Dupuis PR, Yong-Hing K, Cassidy JD, Kirkaldy-Willis WH. Radiologic diagnosis of

degenerative lumbar spinal instability. Spine 1985; 10(3): 262-76.

Dvorak J, Hayek J, Zehnder R. CT-functional diagnostics of the rotatory instability of

the upper cervical spine. Part 2. An evaluation on healthy adults and patients

with suspected instability. Spine 1987; 12(8): 726-31.

Farfan HF. Mechanical disorders of the low back. Philadelphia: Lea & Febiger, 1973;

p247

Farfan HF, Cossette JW, Robertson GH, Wells RV, Kraus H. The effects of torsion on

the lumbar intervertebral joints: the role of torsion in the production of disc

degeneration. J Bone Joint Surg Am 1970; 52(3): 468-97.

Farfan HF, Huberdeau RM, Dubow HI. Lumbar intervertebral disc degeneration: the

influence of geometrical features on the pattern of disc degeneration-a post

mortem study. J Bone Joint Surg Am 1972; 54(3): 492-510.

Graf H. Lumbar instability surgical treatment without fusion: soft system stabilisation.

Rachis 1992; 4: 123-37.

Grobler LJ, Robertson PA, Novotny JE, Pope MH. Etiology of spondylolisthesis.

Assessment of the role played by lumbar facet joint morphology. Spine 1993;

18(1): 80-91.

Gunzburg R, Hutton W, Fraser R. Axial rotation of the lumbar spine and the effect of

flexion. An in vitro and in vivo biomechanical study. Spine 1991; 16(1): 22-8.

Haher TR, O'Brien M, Felmly WT, Welin D, Perrier G, Choueka J, Devlin V, Vassiliou

A, Chow G. Instantaneous axis of rotation as a function of the three columns of

the spine. Spine 1992; 17(6 Suppl): S149-54.

Haughton V, Rogers B, Meyerand M, Resnick D. Measuring the axial rotation of

lumbar vertebrae in vivo with MR imaging. American Journal of

Neuroradiology 2002; 23: 1110-6.

Kirkaldy-Willis WH. The pathology and pathogenesis of low back pain. In: Kirkaldy-

Willis WH editor, Managing low back pain, New York: Churchill Livingstone,

1988; pp. 49-81.

Kirkaldy-Willis WH, Hill RJ. A more precise diagnosis for low back pain. Spine 1979;

4: 102-9.

Kirkaldy-Willis WH, Tchang S. Diagnostic techniques. In: Kirkaldy-Willis WH editor,

Managing low back pain, New York: Churchill Livingstone, 1988; pp. 155-81.

Liu YK, Goel VK, Dejong A, Njus G, Nishiyama K, Buckwalter J. Torsional fatigue of

the lumbar intervertebral joints. Spine 1985; 10(10): 894-900.

Markolf KL. Deformation of the thoracolumbar intervertebral joints in response to

external loads: a biomechanical study using autopsy material. J Bone Joint Surg

Am 1972; 54(3): 511-33.

Page 92: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 4: The Ex vivo CT study

Page IV-17

McFadden KD, Taylor JR. Axial rotation in the lumbar spine and gaping of the

zygapophyseal joints. Spine 1990; 15(4): 295-9.

Mimura M, Panjabi MM, Oxland TR, Crisco JJ, Yamamoto I, Vasavada A. Disc

degeneration affects the multidirectional flexibility of the lumbar spine. Spine

1994; 19(12): 1371-80.

Nachemson A. Lumbar intradiscal pressure. Acta Orthopaedica Scandinavica,

Supplementum 1960; 43: 1-104.

Nachemson A. Lumbar spine instability. A critical update and symposium summary.

Spine 1985; 10(3): 290-1.

Panjabi MM. The stabilizing system of the spine. Part I. Function, dysfunction,

adaptation, and enhancement. J Spinal Disord 1992; 5(4): 383-9; discussion 97.

Pearcy M, Tibrewal S. Axial rotation and lateral bending in the normal lumbar spine

measured by three-dimensional radiography. Spine 1984; 9: 582-87.

Pearcy MJ, Hindle RJ. Axial rotation of lumbar intervertebral joints in forward flexion.

Proc Inst Mech Eng [H] 1991; 205(4): 205-9.

Penning L, Wilmink JT. Rotation of the cervical spine. A CT study in normal subjects.

Spine 1987; 12(8): 732-8.

Pope MH, Frymoyer JW, Krag MH. Diagnosing instability. Clin Orthop Relat Res

1992; (279): 60-7.

Reichmann S. Radiography of the lumbar intervertebral joints. Acta Radiol Diagn

(Stockh) 1973; 14(2): 161-70.

Rohlmann A, Zander T, Schmidt H, Wilke HJ, Bergmann G. Analysis of the influence

of disc degeneration on the mechanical behaviour of a lumbar motion segment

using the finite element method. J Biomech 2006; 39(13): 2484-90.

Schultz AB, Warwick DN, Berkson MH, Nachemson AL. Mechanical properties of

human lumbar spine motion segments. Part 1 responses in flexion, extension,

lateral bending and torsion. Journal of Biomechanical Engineering 1979; 101:

46-52.

Singer K, Svansson G, Day R, Breidahl W, Horrex A. The utility of diagnosing lumbar

rotational instability from twist CT scans. Journal of Musculoskeletal Research

2001; 5: 45-51.

Singer KP, Day RE, Breidahl PD. In vivo axial rotation at the thoracolumbar junction:

an investigation using low dose CT in healthy male volunteers. Clinical

Biomechanics 1989; 4: 145-50.

Tencer AF, Ahmed AM, Burke DL. Some static mechanical properties of the lumbar

intervertebral joint, intact and injured. J Biomech Eng 1982; 104(3): 193-201.

Vrtovec T, Vengust R, Likar B, Pernus F. Analysis of four manual and a computerized

method for measuring axial vertebral rotation in computed tomography images.

Spine 2010; 35(12): E535-41.

Wachowski MM, Mansour M, Lee C, Ackenhausen A, Spiering S, Fanghanel J,

Dumont C, Kubein-Meesenburg D, Nagerl H. How do spinal segments move? J

Biomech 2009; 42(14): 2286-93.

Xia Q, Wang S, Kozanek M, Passias P, Wood K, Li G. In-vivo motion characteristics of

lumbar vertebrae in sagittal and transverse planes. J Biomech 2010; 43(10):

1905-9.

Yong-Hing K, Reilly J, Kirkaldy-Willis WH. The ligamentum flavum. Spine 1976; 1:

226-34.

Page 93: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

CHAPTER 5

Page V-1

The normative cohort MRI study

5.1 Summary

Rotation is frequently implicated as a mechanism by which the anulus fibrosus of the

intervertebral disc (IVD) is injured resulting in herniation of the nucleus pulposus (NP).

There are few data reporting the in vivo mechanical deformation of the NP in response

to sustained rotation. Rotation is coupled with lateral flexion as a composite movement.

Magnetic resonance imaging (MRI) provides a non invasive method of examining NP

deformation by mapping the hydration signal distribution within the IVD.

T1 weighted coronal and sagittal lumbar images and T2 weighted axial images at

L1-2 and L4-5 were obtained from 10 asymptomatic subjects (mean age 29, range: 24 –

34years) in sustained flexed, extended positions plus combined positions of left rotation

with flexion and extension. NP deformation was tracked by mapping the mean change

in hydration profiles from coronal and sagittal pixel measurements. Pooled data were

compared between positions.

An average sagittal change in range of 44° (SD 14.5°) from flexion to extension was

recorded between L1 and S1 (range: 18° – 60°) which resulted in a mean anterior NP

deformation of 16 % of disc hydration profile (range: 3.5% – 19%). On average a 4.8%

coronal deformation of nucleus was recorded when rotation was coupled with either

flexion or extension (SD – 5.1%; range: 0.4% – 15%). Lateral nucleus deformation

direction was variable with respect to left rotation (44% deformed to the left and 56%

deformed to the right). The direction of intersegmental lateral flexion had a more

consistent influence on NP deformation direction with 75% of NPs deforming to the

contralateral side.

Direction of NP deformation following lumbar sagittal plane positional change was

predictable with 19/20 cases deforming towards the opposite direction. Deformation of

the NP following adoption of rotated positions in flexion and extension was reduced in

magnitude and less predictable with respect to direction. In 75% of cases the NP

deformed contralateral to the direction of intersegmental lateral flexion.

Page 94: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 5: The normative cohort MRI study

Page V-2

5.2 Introduction

The intervertebral disc (IVD) is a primary load bearing structure in the lumbar spine,

designed to attenuate compressive force using hydrostatic properties afforded by the

high proteoglycan content of the nucleus pulposus (NP). Offset compressive load will

typically result in deformation towards the area of least compression. The boundary of

the NP is constrained by an intact anulus. However, anular compromise combined with

compressive load may result in symptomatic disc bulge, protrusion or herniation.

Rotation movements are often implicated as an injuring mechanism for the IVD

(O'Sullivan, 2005) especially when performed under load and in a preloaded flexed

position. There is limited ex vivo evidence for the mechanical effect of axial rotation on

the anulus fibrosus (AF) and zygapophysial joints (Adams et al., 1981b; Farfan, 1984;

Farfan et al., 1970) and less again for the in vivo effects on nucleus pulposus

deformation (Fazey et al., 2006).

Lateral flexion and axial rotation are not independent during spinal motion (Cholewicki

et al., 1996; Lovett, 1905.) This biomechanical coupling occurs when primary motion in

either a coronal or axial plane induces secondary motion in the other (White et al.,

1990).

The direction of coupled lumbar segmental motion is controversial and presumed to be

relative to sagittal plane spinal position (Cholewicki et al., 1996; Pearcy et al., 1984a;

Russell et al., 1993). The literature reports coupling patterns are variable in direction

and between intervertebral levels (Panjabi, 1989; Pearcy et al., 1984b; Plamondon,

1988; Vicenzino et al., 1993). Examination of spinal rotation effects must therefore also

include the influence of associated coronal plane motion.

The anatomy of the lumbar spine limits axial rotation to approximately 2°

intersegmentally (Singer et al., 2004). Passive restraint to axial rotation is conferred by

the zygapophysial joints, their ligaments and the intervertebral discs (Adams et al.,

2002). Collagenous fibres of the anulus constrain interbody rotation. Krismer (1996)

reported that selective sectioning of unidirectionally oriented anular fibres resulted in a

2° increase in axial rotation range while bilateral facetectomy resulted in a 1.2° increase

in range. On this basis the anulus was hypothesized to be the primary restraint to

rotation. Others have ascribed control of rotation range to the zygapophysial joints

(Adams et al., 1981a; Shirazi-Adl, 1991; 1994). Torsional stiffness is increased under

Page 95: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 5: The normative cohort MRI study

Page V-3

compressive load (Goodwin et al., 1994) and conversely loss of torsional stiffness

correlates with increased severity of rim lesions in the IVD (Thompson et al., 2000).

Haughton et al (2002) reported a correlation between increased ranges of intersegmental

lumbar rotation in degenerate discs and discogenic pain (Haughton et al., 2002).

Rotation range varies between the upper lumbar segments with sagittally oriented facets

to the lower lumbar segments where facets typically exhibit more coronal orientation

and greater rotation range (Singer et al., 2001).

Segmental rotation range varies with the degree of sagittal plane positioning. Greater

ranges are seen in sub maximal flexion as the facets disengage and are less able to

constrain rotation. Smaller ranges are reported in maximal flexion as ligamentous

structures tighten and forward translation shear engages the articular facets against those

of the subjacent level (Pearcy et al., 1991).

In vivo studies of segmental rotation are technically difficult. Steinman pins inserted

into spinous processes have been used to measure motion (Gregersen et al., 1967;

Gunzberg et al., 1991) however, such invasive methods potentially influence results.

Magnetic resonance imaging provides an elegant, non invasive choice of imaging from

which to measure in vivo deformation of the NP.

Previous studies have used MRI to examine the effect of sagittal plane positioning on

NP movement (Alexander et al., 2007; Beattie et al., 1994; Brault et al., 1997;

Edmondston et al., 2000; Fennell et al., 1996). Different methods were used to track NP

deformation including visual inspection and measurement of the displacement of the

point of maximum pixel intensity relative to changes in subject position.

Axial MR image analysis has demonstrated increased ranges of intersegmental rotation

in normal and degenerate discs (Haughton et al., 2002).

Fazey et al (2006) confirmed a reliable MRI based method to quantify the mean NP

deformation which occurred in response to sagittal position change and rotated positions

of the lumbar spine.

The aim of the present study was to test the consistency with which left rotated postures

influenced NP deformation in positions of flexion and extension at L1-2 and L4-5 using

T2 weighted magnetic resonance imaging. It was hypothesized that in a relatively young

Page 96: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 5: The normative cohort MRI study

Page V-4

normal cohort that the NP would deform in a predictable way relative to sagittal, axial

and conjunct coronal plane segmental positions.

5.3 Methods

Ten asymptomatic subjects, five male and five female with a mean age of 29 years

(range: 24 – 34 years) were recruited to the study. Inclusion criteria sought subjects with

no significant previous history of back pain requiring intervention within the preceding

year, and a body size and shape amenable to positioning within the confines of the MRI.

Subjects were excluded by the presence of any contraindications to MRI including

claustrophobia and the presence of ferrous implants. Institutional Ethics approval was

obtained and all participants provided written informed consent.

Each subject was initially positioned supine on the gantry of 1.5T MR imager (Siemens,

Berlin, Germany). A cylindrical roll of towel was placed under the lordosis to

accentuate extension of the lumbar spine (Figure 5.1A). T1 weighted localizer sagittal

and coronal images (TR/TE [24/6], field of view 400mm, 512x512 matrix) and T2

weighted axial images (TR/TE [5160/102], field of view 210mm, 384x384 matrix) were

acquired with a fast spin echo sequence at the candidate levels L1-2 and L4-5. The

subject was then positioned into left rotation, while maintaining the extended position,

by the addition of a dense foam wedge cushion under the left hemipelvis and image

sequences repeated.

Lumbar spine flexion positioning (Figure 5.1B) prior to image acquisition was achieved

by placement of wedge cushioning under the sacrum and thorax with pillows to support

the flexed cervical spine and knees. Left trunk rotation was induced by the addition of a

wedge cushion under the left hemipelvis in the flexed position.

Intersegmental lateral flexion direction and range was measured on coronal images as

the angle formed by lines extended from superior and inferior end-plates of adjacent

target levels L1-2 and L4-5.

Page 97: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 5: The normative cohort MRI study

Page V-5

Figure 5.1: Subject positioning on the gantry of the MRI. Cylindrical bolster (arrow)

under lumbar spine to induce extension (A) and wedge cushioning under thorax and

sacrum (not visible) to induce flexion (B). (Image used with permission from Clinical

Biomechanics)

Cobb angles were derived from magnified sagittal images from the superior end-plates

of L1 and S1 to measure range of sagittal plane positional change from flexion to

extension (Figure 5.2).

Figure 5.2: Cobb angles (θ) were derived from sagittal images to measure change in

position from extension (A) to flexion (B).

A

B

A B

Page 98: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 5: The normative cohort MRI study

Page V-6

Mid disc axial images for all positions, assumed to optimally represent relative IVD

hydration, were selected for pixel profile analysis (Fazey et al., 2006) (Figure 5.3).

Using imaging software (NIH Image-J, Bethesda, USA) pixel intensity measurements in

sagittal and coronal planes were derived by placing three lines through the mid disc area

from anterior to posterior anulus and from right to left respectively. Raw data were

normalized to 100 points and then averaged within a Labview software routine

(National Instruments, Austin, USA) (Figure 5.3). Averaged line data were then

expressed as a percentage of the whole for each half of the line.

Figure 5.3: Axial images showing orientation and position of 3 lines in coronal and

sagittal planes from which pixel data were derived (A). Raw pixel data for each line

graphed against 100 point scale.

Inter and intra rater reliability was assessed by coefficient of variation (CV) from

repeated measures of Cobb, lateral flexion angles and pixel intensity.

5.4 Results

Acceptable intra rater reliability was demonstrated from repeated measures of all

dependent variables with CV of 3% for Cobb angle and 3.1% and 2.8% for lateral

flexion angles and pixel intensity measurements, respectively.

Obliteration of the contralateral zygapophysial joint space was seen at all levels and

segmental rotation was noted to have occurred in all cases.

The mean difference in position from flexion to extension between L1 and S1, was 44°

(SD 14.5°; range: 18° – 60°), mean lateral flexion range at target levels was 3.4° (SD –

1.85°; range: 0° – 7°).

A B

Page 99: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 5: The normative cohort MRI study

Page V-7

With a change of sagittal plane position from flexion to extension, 19/20 discs

demonstrated a mean anterior NP deformation of 16% (range 3.5% – 19%). One disc

(L4-5) demonstrated a reverse directional trend (8.6%) following moving from an

extended to a flexed position.

The mean coronal offset of NP in the left rotated position was 4.8% of pixel profile

(SD 5.1%; range 0.4% – 15%) irrespective of sagittal plane position with 9 of 20 discs

demonstrating an increased NP offset to the left, and 11 of 20 to the right (Table 5.1).

Mean coronal NP deformation in extension derived from pooled data for both

intervertebral levels was 3.7%. While in flexion this was comparatively greater (mean –

5.9%), the difference was not significant p = 0.08 (Figure 5.4).

Figure 5.4: A trend towards mean coronal NP bias reduction in the extended and left

rotated position was evident at both intervertebral levels though not statistically

significant.

The direction of intersegmental lateral flexion relative to direction of NP bias was

contralateral in 15 discs and ipsilateral in 5 discs (Table 5.1).

Page 100: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 5: The normative cohort MRI study

Page V-8

Table 5.1: Direction and magnitude of NP migration relative to position.

Lumbar Spine Position NP migration direction (n) NP shift (range)

Extension Anterior (19/20) 16% (3.5-19)

Posterior (1/20)

Left Rotation +

Flexion/extension

Left (9/20)

Right (11/20)

5.5% (0.4-15)

5.5 Discussion

The hypothesis that the NP would deform away from the area of primary compression

of the IVD was sustained for sagittal plane supine postures but was more variable in

rotation related to the direction of the associated lateral flexion more than rotation.

Ranges of sagittal plane position change from extension to flexion were comparable to

previous MRI studies though somewhat less than those performed in open magnets.

This difference reflects the spatial constraints within the bore of a conventional magnet.

Axial intersegmental range was assumed to be maximal by obliteration of

zygapophysial joint space on the contralateral side and widening ipsilaterally.

Intersegmental lateral flexion was a secondary coupled response to the primary position

of rotation and therefore not expected to demonstrate full available range.

In the lumbar spine each degree of segmental axial rotation is accompanied by two

degrees of lateral flexion (Cholewicki et al., 1996) therefore it is not unexpected that the

lateral flexion component of the composite position would have the greater effect on NP

deformation.

Hydrated discs behave as a hydrostatic mechanism and as such will deform towards an

area of least load. Compressive force being greater on the side of concavity, the

expectation is for deformation of the NP towards the convexity (Périé et al., 2001;

Violas et al., 2005).

This study, however, revealed that 75% of NPs examined deformed towards the coronal

plane convexity in the rotated position and 19/20 (95%) towards the sagittal plane

convexity in the extended position. Some previous studies have reported similar NP

behaviour in response to sagittal plane position and suggested that predictability may be

reduced in the presence of degenerative change (Edmondston et al., 2000; Schnebel et

al., 1988). In the current study, the single NP that deformed posteriorly in extension did

not exhibit visual features of degenerative change. It may be speculated that greater

tensile force generated in the capsular portion of the anterior anulus than that of the

Page 101: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 5: The normative cohort MRI study

Page V-9

compressive force posteriorly will result in deformation towards the area of

compressive load. Further study comparing tensile and compressive forces within the

IVD would be required to test this hypothesis.

Reduced NP deformation magnitude reported at both intervertebral levels in extension

plus left rotation may reflect reduced range of available segmental axial rotation in

extended positions (Haberl, 2004). Additionally, increased range of lumbar segmental

axial rotation has been demonstrated in submaximal flexion (Pearcy et al., 1991) and

may contribute to observed differences.

The variable NP deformation in left rotated postures may relate to the scanning

methodology.

Previous studies profiled peak pixel points from a single line through the mid disc,

assuming these to represent the centre of the NP and therefore a consistent point for

inter-individual comparison (Alexander et al., 2007; Edmondston et al., 2000).

Observation of graphed pixel intensity frequently reveals numerous points of higher

pixel intensity representing relative hydration, even when data from three lines were

averaged. A methodology such as that employed in the current study that calculates

strength of hydration signal offset from multiple samples rather than a single point, may

therefore be more representative of NP deformation patterns.

Although speculative, results of this preliminary normative study may have implications

for the contribution of rotation and lateral flexion to lumbar disc injury and patterns of

disc herniation. Axial rotated positions in supine appear to have a less predictable effect

on NP deformation, than lateral flexion. It may therefore be of interest to determine the

relationship between injuring mechanisms and herniation patterns in symptomatic

individuals.

Study limitations include the confines of the MR constraining sagittal range of motion

to sub maximal. Segemental lateral flexion, as a secondary response to primary rotation,

was unlikely to be to the maximum available range. Disc sampling for hydration

profiling was limited to two dimensions; three dimensional imaging would enable a

composite analysis of the entire target disc. Imaging was commenced with subject pre

positioning in the sagittal plane. Data derived from this position was compared with that

of the subsequent combined positioning. Imaging and analysis of NP hydration

weighting in the resting neutral position would provide greater insight into the

Page 102: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 5: The normative cohort MRI study

Page V-10

comparative deformation by excluding any effect of pre positioning on the IVD. Data

derived from coronal images for lateral flexion direction and magnitude may be

influenced by slice orientation. A slice angle posterior to the axis of motion may

partially reflect sagittal plane position. The likelihood of this is increased with regional

rotation. Future investigations should employ coronal images adjusted to each scanned

level.

A future study would be recommended to test the effect of primary coronal plane

positioning into lateral flexion to more accurately determine comparative predictability

of NP deformation direction between coronal and axial plane postures.

5.6 Conclusions

This study has shown that in young asymptomatic individuals the NP at L1-2 and L4-5

deforms predictably away from offset compressive load in positions of flexion and

extension. The direction of NP deformation following left rotation in flexion and

extension is unpredictable. Deformation relative to the direction of secondary

intersegmental lateral flexion is more predictable as 75% of cases deformed away from

the direction of lateral flexion.

Page 103: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 5: The normative cohort MRI study

Page V-11

References

Adams M, Bogduk N, Burton K, Dolan P. The Biomechanics of Back Pain. London,:

Churchill Livingstone, 2002.

Adams M, Hutton W. The relevance of torsion to the mechanical derangement of the

lumbar spine. Spine 1981a; 6: 241-8.

Adams MA, Hutton WC. The relevance of torsion to the mechanical derangement of the

lumbar spine. Spine 1981b; 6(3): 241-8.

Alexander LA, Hancock E, Agouris I, Smith FW, MacSween A. The response of the

nucleus pulposus of the lumbar intervertebral discs to functionally loaded

positions. Spine 2007; 32(14): 1508-12.

Beattie PF, Brooks W, Rothstein J. Effect of lordosis on the position of the nucleus

pulposus in supine subjects. Spine 1994; 19: 2096-102.

Brault J, Driscoll D, Laakso L, Kappler R, Allin E, Glonek T. Quantification of lumbar

intradiscal deformation during flexion and extension by mathematical analysis

of magnetic resonance imaging pixel intensity profiles. Spine 1997; 22: 2066-

72.

Cholewicki J, Crisco J, Oxland T, Yamamoto I, Panjabi M. Effects of posture and

structure on three- dimensional coupled rotations in the lumbar spine. A

biomechanical analysis. Spine 1996; 21: 2421-8.

Edmondston S, Song S, Bricknell R, Davies P, Fersum K, Humphries P, Wickendon D,

Singer K. MRI evaluation of lumbar spine flexion and extension in

asymptomatic individuals. Manual Therapy 2000; 5: 158-64.

Farfan HF. The torsional injury of the lumbar spine. Spine (Phila Pa 1976) 1984; 9(1):

53.

Farfan HF, Cossette JW, Robertson GH, Wells RV, Kraus H. The effects of torsion on

the lumbar intervertebral joints: the role of torsion in the production of disc

degeneration. J Bone Joint Surg Am 1970; 52(3): 468-97.

Fazey P, Song S, Mønsas A, Johansson L, Haukalid T, Price R, Singer K. An MRI

investigation of intervertebral disc deformation in response to torsion. Clinical

Biomechanics 2006; 21: 538-42.

Fennell A, Jones A, Hukins D. Migration of the nucleus pulposus within the

intervertebral disc during flexion and extension of the spine. Spine 1996; 21:

2753- 7.

Goodwin R, James K, Daniels A, Dunn H. Distraction and compression loads enhance

spine torsional stiffness. Journal of Biomechanics 1994; 27(8): 1049-57.

Gregersen G, Lucas D. In vivo study of the axial rotation of the human thoracolumbar

spine. Journal of Bone and Joint Surgery (British volume) 1967; 49: 247-62.

Gunzberg R, Hutton W. Axial rotation of the lumbar spine and the effect of flexion: An

in vitro and in vivo biomechanical study. Spine 1991; 16(1): 22- 8.

Haberl H. Kinematic response of lumbar functional spinal units to axial torsion with and

without superimposed compression and flexion/extension. European Spine

Journal 2004; 13(6): 560-6.

Haughton V, Rogers B, Meyerand M, Resnick D. Measuring the axial rotation of

lumbar vertebrae in vivo with MR imaging. American Journal of

Neuroradiology 2002; 23: 1110-6.

Krismer M, Haid C, Rabl W. The contribution of anulus fibers to torque resistance.

Spine 1996; 21(22): 2551- 7.

Lovett R. The mechanism of the normal spine and its relation to scoliosis. Boston

Medical and Surgical Journal 1905; 153: 349-58.

Page 104: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 5: The normative cohort MRI study

Page V-12

O'Sullivan P. Diagnosis and classification of chronic low backpain disorders:

Maladaptive movement and motor control impairments as underlying

mechanism. Manual Therapy 2005; 10: 242-55.

Panjabi M. How does posture affect coupling in the lumbar spine? Spine 1989; 14:

1002-11.

Pearcy M, Hindle R. Axial rotation of lumbar intervertebral joints in forward flexion.

Proc Inst Mech Eng [H] 1991; 205(4): 205-9.

Pearcy M, Portek I, Shepherd J. Three-dimensional x-ray analysis of normal movement

in the lumbar spine. Spine 1984a; 9(3): 294-7.

Pearcy M, Tibrewal S. Axial rotation and lateral bending in the normal lumbar spine

measured by three-dimensional radiography. Spine 1984b; 9: 582-87.

Périé D, Sales De Gauzy J, Curnier D, Hobatho M. Intervertebral disc modeling using a

MRI method : migration of the nucleus zone within scoliotic intervertebral discs.

Magnetic Resonance Imaging 2001; 19(9): 1245-8.

Plamondon A. Application of a stereoradiographic method for the study of

intervertebral motion. Spine 1988; 13: 1027-32.

Russell P, Pearcy MJ, Unsworth A. Measurement of the range and coupled movements

observed in the lumbar spine. Br J Rheumatol 1993; 32(6): 490-7.

Schnebel B, Simmons J, Chowning J, Davidson R. A digitising technique for the study

of movement of intradiscal dye in response to flexion and estension of the

lumbar spine. Spine 1988; 13: 309-12.

Shirazi-Adl A. Finite element evaluation of contact loads on facets of a L2-L3 lumbar

segment in complex loads. Spine 1991; 16: 533-41.

Shirazi-Adl A. Non linear stress analysis of the whole lumbar spine in torsion -

mechanics of facet articulation. Journal of Biomechanics 1994; 27: 289-99.

Singer K, Boyle J, Fazey P. Comparative anatomy of the zygapophysial joints, Grieve’s

Modern Manual Therapy, Edinburgh: Churchill Livingstone, 2004.

Singer K, Svansson G, Day R, Breidahl W, Horrex A. The utility of diagnosing lumbar

rotational instability from twist CT scans. Journal of Musculoskeletal Research

2001; 5: 45-51.

Thompson R, Pearcy M. Disc lesions and the mechanics of the intervertebral joint

complex. Spine 2000; 25: 3026-35.

Vicenzino G, Twomey L. Sideflexion and induced lumbar spine conjunct rotation and

its influencing factors. Australian Journal of Physiotherapy 1993; 39: 299-306.

Violas P, Estivalezes E, Pedrono P, Sales de Gauzy J, Sevely A, Swider P. A method to

investigate intervertebral disc morphology from MRI in early idiopathic

scoliosis: a preliminary evaluation in a group of 14 patients. Magnetic

Resonance Imaging 2005; 23: 475-9.

White A, Panjabi M. Clinical Biomechanics of the Spine, 2 ed. Philadelphia: Lippincott,

1990;

Page 105: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

CHAPTER 6

Page VI-1

The lateral flexion cohort MRI study

6.1 Summary

While there are numerous studies examining aspects of sagittal plane motion in the

lumbar spine, few consider coronal plane range of motion and there are no in vivo

reports of the response of nucleus pulposus (NP) displacement in lateral flexion. This

study quantified in vivo NP deformation in response to side flexion in healthy

volunteers. Concomitant lateral flexion and axial rotation range were also examined to

evaluate the direction and extent of NP deformation.

Axial T2 and coronal T1 weighted Magnetic Resonance Images (MRI) were obtained

from 21 subjects (mean age: 24.8 years) from L1 to S1 in the neutral and left laterally

flexed position. Images were evaluated for intersegmental ranges of lateral flexion and

axial rotation. A novel method derived linear pixel samples across the width of the disc

from T2 images, from which the magnitude and direction of displacement of the NP

was determined. This profiling technique represented the relative hydration pattern

within the disc.

The NP was displaced away from the direction of lateral flexion in 95/105 discs

(p<0.001). The extent of NP displacement was associated strongly with lateral flexion at

L2-3 (p<0.01). The greatest range of lateral flexion occurred at L2-3, L3-4 and L4-5.

Small intersegmental ranges of axial rotation occurred at all levels but were not

associated with NP displacement.

The direction of NP deformation was highly predictable in laterally flexed healthy

lumbar spines; however, the magnitude of displacement was not consistent with the

degree of intersegmental lateral flexion or rotation.

Page 106: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 6: The lateral flexion cohort study

Page VI-2

6.2 Introduction

An increased knowledge of lumbar spine pathomechanics has improved our

understanding of the cause and effect of low back pain. However, a major focus has

been on sagittal plane motion, particularly flexion, on the assumption that this

represents the most functional lumbar motion (Adams et al., 2002). Sagittal motion also

contributes the greatest directional range and is most often implicated as an injuring

mechanism (Pearcy et al., 1984a). Axial and coronal plane motions, however, are

important components of spinal segmental mobility but have not attracted the same

attention in the literature due to the complexities of coupled motion.

Existing literature focuses on regional range of coronal plane motion (Kachingwe et al.,

2005; Schuit et al., 1997) and on functional consequences related to sports (Burnett et

al., 1998). Earlier studies on intersegmental range (Dvorak et al., 1991; Pearcy et al.,

1984b) provide limited insight into the mechanics of lateral flexion. Little consideration

is given to the effect of lateral flexion on the intervertebral disc (IVD). As IVD

dimensions in the coronal plane are approximately 50% greater than in the sagittal plane

it is reasonable to infer that lateral movement will generate higher stress distributions

within the IVD than sagittal displacement (Adams et al., 2002). Combinations of

movement in both planes can generate very high intradiscal and anular tensile strains

especially when combined with axial rotation (Steffen et al., 1998) and as such are

implicated in injury (Adams et al., 2002; Scannell et al., 2009).

Lateral flexion and axial rotation are coupled movements within the lumbar spine

(White et al., 1990). It is well known that primary movement in one plane induces

movement in the other, likely through the combined influence of bony architecture,

intervertebral disc, ligamentous compliance and muscle action (Scholten et al., 1985).

However dispute exists over the relationships between axial and coronal plane

contributions (Legaspi et al., 2007). Despite this, assessment of motion in one direction

should give due consideration to the other.

The nucleus pulposus (NP) by virtue of high proteoglycan content, acts hydrostatically

to attenuate load through the disc and distribute force to the anulus and end plates.

Examination of hydration profiles within the NP can therefore reflect deformation

patterns in response to offset loading. Several in vivo studies of healthy individuals,

employing Magnetic Resonance Imaging (MRI), have reported IVD deformation in the

sagittal and axial plane (Brault et al., 1997; Edmondston et al., 2000; Fazey et al., 2006;

Page 107: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 6: The lateral flexion cohort study

Page VI-3

Fennell et al., 1996) and in scoliosis (Périé et al., 2001). Limited data on NP

deformation in lateral flexion exist mainly from cadaver studies (Tsantrizos et al.,

2005); however, no investigations to date have reported in vivo NP deformation in

response to induced lateral flexion.

MRI provides an elegant method of examining NP response to postural changes of the

spine. Novel methods of image analysis using T2 weighted MRI images have

previously been used to quantify NP deformation (Fazey et al., 2006). This hypothesis

generating study sought to quantify in vivo NP deformation in response to side bending

in healthy volunteers. Additionally, the association between lateral flexion and axial

rotation range were examined to evaluate the direction and extent of NP deformation.

6.3 Methods

A total of 21 healthy volunteers were recruited to the study; 11 female and 10 male,

with a mean age of 24.8 years (range: 20-34). Exclusion criteria included

contraindications to MRI or significant degenerative disc disease as assessed by two

orthopaedic surgeons (Y.I & Y.S.). Prior to the study, institutional ethics approval was

obtained and each subject provided written consent.

Subjects were initially positioned supine on the gantry of a 0.2T horizontally open MRI

unit (AIRIS mate, Hitachi Inc., Sopporo, Japan). The gantry was inserted into the

magnet and a series of T1 and T2 weighted images acquired first in the supine neutral

position then, following re-positioning, sequences were repeated in the laterally flexed

posture.

The axial T2 relaxation sequences were acquired through the mid disc region from L1-2

to L5-S1 with a fast spin echo sequence (3120/120 (TR/TE), FOV 260), 8mm slice

thickness and an acquisition time of 6:52 min. Slice position was manually determined

from planning images and the slice thickness was optimised at each segment to sample

the disc volume.

The pelvis was then stabilised with a strap to prevent rotation and the subject was

positioned into left side bending with one assistant manually holding the knees to

prevent lateral movement. The subjects were then asked to actively laterally flex to the

limit of their range. A second assistant applied overpressure at the shoulders to

minimise trunk rotation and to achieve a limit of lateral flexion range, which was

Page 108: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 6: The lateral flexion cohort study

Page VI-4

maintained passively by the assistants during imaging. Mid disc image sequences at all

levels were repeated using the same parameters.

To evaluate segmental rotation, axial T1 weighted images were taken through the bony

vertebra of L1 to S1 using a fast spin echo sequence (385/24.5 (TR/TE), FOV 300) slice

thickness 6mm, acquisition time 5:45 min. Finally coronal T1 images (285/24.5

(TR/TE), FOV 300; 6mm thickness, 1:34 min), which were optimal for demonstration

of the bony anatomy, were used to examine lateral flexion (Figure 6.1).

Figure 6.1: Coronal T1 weighted image demonstrating lumbar spine lateral flexion

achieved by subject positioning.

6.3.1 Image analysis

From the T1 axial images, rotation angles were calculated by a line from the spinous

process of each vertebra to the midpoint of the vertebral body. The vertical image frame

was referenced as the sagittal plane and the angle subtended between each was recorded

as the degree of axial rotation of that segment. For the S1 segment a line taken from the

sacral promontory to the mid point of the S1 body was extended posteriorly (Figure

6.2A).

Page 109: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 6: The lateral flexion cohort study

Page VI-5

Figure 6.2: Calculation of lumbar segment rotation angles from axial images (A) and

modification of the Cobb method for calculating segmental lateral flexion angles (B).

Lateral flexion intersegmental angles were calculated from the T1 weighted coronal

images. Using image analysis software (NIH Image-J, Bethesda, USA), the corners of

each vertebral body from L1 to L5 were identified and marked. The angle was then

measured at the intersection of the lines extending through the midpoints between the

two anterior and two posterior corners (Figure 6.2B). Derived angles were measured

twice by two blinded assessors resulting in high reliability (ICC 0.99).

Direction of NP deformation was derived from the neutral and laterally flexed T2

weighted mid-disc axial images using a previously described technique (Fazey et al.,

2006) and image analysis software (NIH Image-J, Bethesda, USA). This technique

enabled pixel intensity profiling to represent the relative hydration pattern within the

disc.

On neutral and laterally flexed axial images at each intervertebral level from L1-2 to

L5-S1, three lines were placed across the mid-disc region from right to left (Figure 6.3).

Raw pixel data from these line samples were normalised to 100 points, averaged using a

Labview software routine (National Instruments, Austin, USA), then imported into

Excel where the direction, extent and pattern of hydration was derived for neutral and

laterally flexed image pairs.

Page 110: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 6: The lateral flexion cohort study

Page VI-6

The NP did not consistently show a symmetrical profile in the neutral position.

Inevitably there was a small directional offset of the NP to either side. This variable was

taken into account in the calculations for NP deformation direction and extent.

Figure 6.3: Measurement of pixel intensity in neutral and laterally flexed positions.

Averaged pixel data were sampled from three coronal lines per segment from the paired

T-2 weighted axial images to represent the relative hydration pattern of the NP. Trunk

rotation, although minimised, results in visible segmental rotation in the laterally flexed

position.

Descriptive statistics were used to inspect the data for the direction and extent of NP

deformation, in addition to lateral flexion and rotation range at lumbar levels: L1-2 to

L5-S1. Direction of NP deformation in response to posture and segmental level was also

recorded. Unpaired t-tests were used to determine whether a gender difference in

flexibility was present. The NP position in neutral and lateral flexion was compared

using a paired t-test. Differences in lateral flexion angles between levels were examined

using ANOVA. Finally, simple linear regression was used to test for associations

between i) segmental lateral flexion and ii) NP deformation and lateral flexion. In all

statistical tests a probability of p<0.05 was used as the criterion to record significant

differences.

Page 111: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 6: The lateral flexion cohort study

Page VI-7

6.4 Results

There was no difference between genders for lateral flexion range of motion (p=0.47)

therefore data were pooled for subsequent analyses. A summary of the results for side

flexion, coincident rotation, and the extent and direction of the NP deformation for L1-2

to L5-S1 segmental levels, is provided in Table 6.1. In 95% of all cases a right sided NP

deformation occurred in response to end-range left side flexion, the exceptions were

found primarily at L5-S1.

There was a significant difference at all segmental levels contrasting the NP pixel

intensity position adopted in the side flexion compared with neutral axial images

(p<0.001) (Figure 6.4). The most pronounced change in the deformation of the nucleus

position was recorded for L2-3, L3-4 and L4-5 (Figure 6.4). There was a moderate

association between the magnitude of side-flexion and NP deformation only at L2-3

(r=0.54, p<0.01) (Table 6.1).

The greatest side flexion range was demonstrated at L3-4 and L4-5 (Figure 6.4) which

were significantly different from other adjacent levels (p<0.005). Coincident rotation

was small in contrast and showed no association with side flexion range (Figure 6.4).

Table 6.1: Summary of lumbar mobility and internal disc deformation responses to

sustained left side flexion in healthy volunteers

L1-2 L2-3 L3-4 L4-5 L5-S1

Side bend (°)

Mean (SD)

5.2 (2.24) 6.7 (2.22) 6.7 (1.64) 6.7 (3.48) 5.4 (3.86)

Rotation (°)

Mean (SD)

0.01 (1.97) 0.96 (2.13) 0.38 (1.74) 0.24 (2.07) 0.68 (2.78)

NP deformation

(percentage)

11.3

(9.75)

18.2

(11.0)

22.5

(7.1)

22.1

(7.95)

7.9

(9.86)

NP direction

(percentage)

21/21

(100%)

20/21

(95%)

21/21

(100%)

21/21

(100%)

18/21

(81%)

The apical segments showed the greatest displacement of the NP which was mirrored in

part by the relative extent of side-flexion. There were no associations between NP

deformation and the segmental axial rotation.

Page 112: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 6: The lateral flexion cohort study

Page VI-8

Figure 6.4: Inter-relationships between segmental side-flexion, coincident rotation and

the extent of NP deformation following unilateral sustained left side flexion position.

Marked change occurred in the apical segments.

6.5 Discussion

This study, involving young, asymptomatic subjects, sought to quantify NP deformation

in response to side flexion and to examine side flexion and segmental rotation range

relative to a lateral NP deformation.

The results showed a strong correlation between direction of NP deformation and

direction of lateral flexion, with 95% of segments (100/105) deforming towards the

contralateral side of lateral flexion. The directional relationship between NP

deformation and lateral flexion was expected to be strong, assuming a predictable

hydrostatic behaviour of the NP as it attenuates load in the healthy disc (Adams et al.,

1994). It was of interest to note that five IVDs deformed towards the side of lateral

flexion. Four of these occurred at L5-S1, where smaller ranges of lateral flexion were

recorded (mean: 5.4°), and one at L2-3.

From the MRI assessment, there was a significant shift of NP signal intensity away

from the neutral position away the direction of side bending, with a mean deformation

of 22.5%. There was a significant correlation between the magnitude of NP

deformation and range of lateral flexion at L2-3.

T2-weighted MRI images have been used to map NP hydration profiles in response to

changes in spinal posture. Pixel histograms of single (Edmondston et al., 2000) or

Page 113: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 6: The lateral flexion cohort study

Page VI-9

averaged data (Fazey et al., 2006) have elaborated the putative effect of postural

adaptations on IVD hydrostatic behaviour.

Hydration, and therefore signal intensity, as represented from T2-weighted images is

not uniform across the IVD or even within the NP. Methods of measuring pixel

intensity from a single sample across the IVD may be relatively insensitive to the

overall hydration change, particularly if the sampling profiles are not representative of

the IVD.

The greatest range of lateral flexion range occurred at the apex of the lateral curve, L2-

3, L3-4, and the least at the upper and lower limits of the curve. Studies by Pearcy et al

(Pearcy et al., 1984a; Pearcy et al., 1984b), using biplanar radiography of volunteers in

erect standing, have reported smaller segmental ranges of motion in lateral flexion than

the current study but greater ranges at L5-S1 and L1-2. This difference may reflect

supine positioning within the confines of the MRI in which the pelvis and lower limbs

were stabilised while lateral flexion was induced via shoulder and thoracic spine

movement. Such positioning may potentially limit the available range at the

lumbosacral junction and upper lumbar spine. Additionally, there is a tendency for the

spine to demonstrate a correction to neutral at the curve inflexion points which lie close

to the transitional levels. This phenomenon is illustrated in a balanced thoracolumbar

scoliosis curve where the inflexion vertebrae show a neutral disc alignment.

Segmental rotation ranges were small by comparison to previous studies (Pearcy et al.,

1984b). This finding most likely reflects subject positioning into lateral flexion where

rotation was only a secondary response. Care should be taken not to over interpret these

findings with respect to coupling patterns given the constrained nature of the

positioning used in the present study. Reports of associations between coronal and axial

plane motion provide no consensus as to the directional influence of one motion over

the other (Legaspi et al., 2007).

There are a number of limitations to this study which have the potential to influence the

interpretation of these data. Measurement errors may arise with the small ranges of

lateral flexion and NP deformation, particularly at L5-S1, and the relative initial resting

position of the NP. However, repeated assessment showed acceptable accuracy.

Page 114: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 6: The lateral flexion cohort study

Page VI-10

Additionally, it is known that 20-25% of the population demonstrate evidence of mild

physiological scoliosis (Grivas et al., 2008). A pre-existing degree of scoliosis would

inevitably influence both the NP position in neutral, and the potential range of both

lateral flexion and axial rotation. Available side flexion range may be compromised due

to the coupled rotation. It would be of interest to examine the influence of scoliosis in

future studies and map the association between NP deformation and the magnitude of

the deformity.

There was no significant correlation between rotation range and NP deformation. This is

not unexpected given the small ranges of rotation demonstrated. Further elaboration of

this in future studies, where rotation was unconstrained, would help define the extent of

association between both elements of coupled motion.

This study was limited to young subjects with no history of back pain or macroscopic

degenerative change on MRI. Future studies could consider the response of anular

injury and degenerative changes of the IVD to end-range side bending and rotation

using this MRI based technique of hydration mapping.

The technique employed in the current study involved three line samples across the IVD

to integrate and average the assessment of directional NP deformation. More complex

3-D profile maps of the anulus and NP would confer an improved evaluation of

hydration patterns across the entire intervertebral disc (Haughton, 2006; Périé et al.,

2001) as illustrated in Figure 6.5.

It would be of interest to replicate this study in an open magnet MR imager, which

would permit both physiological axial loading and unconstrained lateral flexion. More

accurate consideration of conjunct rotation and coupling patterns would then be

possible.

Page 115: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 6: The lateral flexion cohort study

Page VI-11

Figure 6.5: Relatively symmetrical 3-D profile of the NP in neutral (right) in contrast to

the profile derived in side flexion (left). Surface intensity plots of the NP emphasise the

displacement of the side flexed NP (left) away from the neutral position.

6.6 Conclusion

This study has demonstrated that the NP deforms in a predictable direction towards the

convexity in a laterally flexed lumbar spine. There was a significant degree of change in

NP hydration pattern between the neutral and laterally flexed position, most pronounced

at the mid lumbar levels and less so at L1-2 and L5-S1. The degree to which the NP

deforms generally correlates with the degree of segmental lateral flexion. Axial rotation,

occurring concomitantly with primary lateral flexion, did not correlate with NP

deformation or lateral flexion range. In this study physiological coupling patterns of the

lumbar segments cannot be inferred as side flexion was constrained.

Page 116: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 6: The lateral flexion cohort study

Page VI-12

References

Adams M, Bogduk N, Burton K, Dolan P. The Biomechanics of Back Pain. London,:

Churchill Livingstone, 2002.

Adams M, McNally D, Chinn H, Dolan P. Posture and the compressive strength of the

lumbar spine. Clinical Biomechanics 1994; 9: 5-14.

Brault J, Driscoll D, Laakso L, Kappler R, Allin E, Glonek T. Quantification of lumbar

intradiscal deformation during flexion and extension by mathematical analysis

of magnetic resonance imaging pixel intensity profiles. Spine 1997; 22: 2066-

72.

Burnett AF, Barrett CJ, Marshall RN, Elliott BC, Day RE. Three-dimensional

measurement of lumbar spine kinematics for fast bowlers in cricket. Clin

Biomech (Bristol, Avon) 1998; 13(8): 574-83.

Dvorak J, Panjabi MM, Chang DG, Theiler R, Grob D. Functional radiographic

diagnosis of the lumbar spine. Flexion-extension and lateral bending. Spine

1991; 16(5): 562-71.

Edmondston S, Song S, Bricknell R, Davies P, Fersum K, Humphries P, Wickendon D,

Singer K. MRI evaluation of lumbar spine flexion and extension in

asymptomatic individuals. Manual Therapy 2000; 5: 158-64.

Fazey P, Song S, Mønsas A, Johansson L, Haukalid T, Price R, Singer K. An MRI

investigation of intervertebral disc deformation in response to torsion. Clinical

Biomechanics 2006; 21: 538-42.

Fennell A, Jones A, Hukins D. Migration of the nucleus pulposus within the

intervertebral disc during flexion and extension of the spine. Spine 1996; 21:

2753- 7.

Grivas TB, Vasiliadis ES, Mihas C, Triantafyllopoulos G, Kaspiris A. Trunk asymmetry

in juveniles. Scoliosis 2008; 3: 13.

Haughton V. Imaging intervertebral disc degeneration. J Bone Joint Surg Am 2006; 88

Suppl 2: 15-20.

Kachingwe AF, Phillips BJ. Inter- and intrarater reliability of a back range of motion

instrument. Arch Phys Med Rehabil 2005; 86(12): 2347-53.

Legaspi O, Edmond SL. Does the evidence support the existence of lumbar spine

coupled motion? A critical review of the literature. J Orthop Sports Phys Ther

2007; 37(4): 169-78.

Pearcy M, Portek I, Shepherd J. Three-dimensional x-ray analysis of normal movement

in the lumbar spine. Spine 1984a; 9(3): 294-7.

Pearcy M, Tibrewal S. Axial rotation and lateral bending in the normal lumbar spine

measured by three-dimensional radiography. Spine 1984b; 9: 582-87.

Périé D, Sales De Gauzy J, Curnier D, Hobatho M. Intervertebral disc modeling using a

MRI method : migration of the nucleus zone within scoliotic intervertebral discs.

Magnetic Resonance Imaging 2001; 19(9): 1245-8.

Scannell JP, McGill SM. Disc prolapse: evidence of reversal with repeated extension.

Spine 2009; 34(4): 344-50.

Scholten P, Veldhuizen A. The influence of spine geometry on the coupling between

lateral bending and axial rotation. Engineering in Medicine 1985; 14: 167-71.

Schuit D, Petersen C, Johnson R, Levine P, Knecht H, Goldberg D. Validity and

reliability of measures obtained from the OSI CA-6000 Spine Motion Analyzer

for lumbar spinal motion. Man Ther 1997; 2(4): 206-15.

Steffen T, Baramki H, Rubin R, Antoniou J, Aebi M. Lumbar intradiscal pressure

measured in the anterior and posterolateral annular regions during asymmetrical

loading. Clinical Biomechanics 1998; 13: 495-505.

Page 117: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 6: The lateral flexion cohort study

Page VI-13

Tsantrizos A, Ito K, Aebi M, Steffen T. Internal strains in healthy and degenerated

lumbar intervertebral discs. Spine 2005; 30(19): 2129-37.

White A, Panjabi M. Clinical Biomechanics of the Spine, 2 ed. Philadelphia: Lippincott,

1990.

Page 118: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

CHAPTER 7

Page VII-1

The older cohort MRI study

7.1 Summary

Intervertebral disc (IVD) degeneration is common and associated with age. Increased

ranges of lumbar intersegmental rotation have been associated with IVD degeneration.

Nucleus pulposus (NP) deformation in response to offset compressive loading has been

reported in flexed, extended and rotated postures. However, predictability of

deformation direction is uncertain in the presence of degeneration. The aim of this study

was to measure the magnitude and determine the direction and predictability of in vivo

lumbar NP deformation in older subjects placed in a rotated position within an MRI

scanner.

Eleven healthy subjects (5 female, 6 male) with a mean age of 48.4 (range: 40 – 57)

were imaged in neutral then left rotated postures employing mid-disc axial T2 and

coronal T1 weighted image sequences from L1-2 to L5-S1. Images were analysed for

direction and magnitude of NP deformation relative to rotation using a pixel profiling

technique, then compared with stage of IVD degeneration, and direction and angle of

concomitant segmental lateral flexion.

Mean NP deformation was 2.1% of disc width. At L3-4 there was a modest association

between lateral flexion and NP deformation (r=0.38, p<0.034). In the left rotation

position 47.3% of all discs deformed to the left and 52.7% to the right; 61.8% deformed

contralateral to the direction of intersegmental lateral flexion. NP deformation direction

was independent of level, grade of degeneration or segmental lateral flexion range.

In older subjects the direction of nucleus deformation was unpredictable relative to

rotation and poorly predictable relative to lateral flexion direction. The degree of

degeneration did not appear to be associated with predicting the deformation direction.

Page 119: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 7: The older cohort study

Page VII-2

7.2 Introduction

Degenerative or age related changes are prevalent in the lumbar spine, affecting 31% of

15 year olds (Salminen et al., 1993) and 100% of 50 year olds (Adams et al., 2002).

Lower lumbar segments typically show a greater extent of degenerative changes.

Biomechanically, moderate degenerative change has been demonstrated to be associated

with increased ranges of intersegmental rotation in the lumbar spine and severe

degeneration with decreased range (Haughton et al., 2002; Johansen et al., 1999).

Degeneration was putatively related to torsional strain by Farfan (Farfan et al., 1970)

who noted that anular lesions induced experimentally by torsion in cadaver spines were

identical in nature to those seen in degenerated discs. Farfan et al therefore hypothesised

that: degeneration was related more with rotational rather than compressive forces in

vivo, and that the greater ranges of intersegmental rotation seen at degenerated levels

compared with non degenerated levels may be interpreted as causative.

The pathophysiology of degeneration has been extensively studied and reviewed

(Hadjipavlou et al., 2008). It has a complex and multifactorial aetiology across the

spectrum of age, genetics, nutrition, metabolic, infection and mechanical influences.

This process of degeneration may precipitate anular tears and disc herniation which

disrupt the intradiscal environment and result in reduced capacity to attenuate

compressive load via the nucleus pulposus (NP) (Adams et al., 2010).

Magnetic Resonance imaging has been used to grade fluid loss and end plate changes

by analysis of T2 weighted signal changes with reference to normals (Jensen et al.,

2009; Jensen et al., 2008; Luoma et al., 2001).

Signal strength on T2 weighted MR images has been shown to be an accurate method

for assessing IVD hydration and potentially a more accurate measure of disc

degeneration than disc height (Haughton, 2006; Luoma et al., 2001).

It has been speculated that NP migration direction, a normal response to offset

compressive loading, is not consistent in sagittal plane postures of the lumbar spine

(Edmondston et al., 2000). However, there is preliminary in vivo evidence for

directionality of deformation in young normal lumbar spines positioned supine in left

rotation, albeit combined with flexion or extension (Fazey et al., 2006). No evidence

exists for the direction, magnitude or predictability of NP deformation in response to

rotated positions in the lumbar spines of older subjects.

Page 120: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 7: The older cohort study

Page VII-3

The purpose of this study was to measure the magnitude and determine the direction

and predictability of in vivo NP deformation using MRI in middle aged subjects

positioned into a rotated posture. It was hypothesised that greater intersegment lateral

flexion would induce the largest NP deformation from the neutral position; that more

severe disc degeneration would reduce the extent of NP deformation following axial or

coronal plane positioning and that the NP would deform contralaterally to the direction

of segmental lateral flexion.

7.3 Methods

11 healthy volunteers were recruited to the study; five female and six male with a mean

age of 48.4 years (range: 40 – 57). Exclusion criteria included general contraindications

to MRI and troublesome back pain requiring treatment within the past 12 months.

Written consent from each subject and institutional ethics approval were obtained.

Subjects were positioned on the gantry of a 1.5T MRI unit (Siemens, Berlin, Germany)

in supine followed by left rotated positions. A series of T2 weighted sagittal, axial and

T1 coronal image sequences were acquired. Axial T2 weighted neutral images were

obtained through the mid-disc region from L1-2 to L5-S1 using a fast spin echo

sequence (TR/TE [3020/102.0], field of view 20.9x16.7cm, 306x384 matrix, 4mm slice

thickness).

Coronal T1 weighted images were also obtained at each candidate level with a fast spin

echo sequence (TR/TE [619.0/11.0], field of view 30x30cm, 448x448 matrix, 4mm

slice thickness). The coronal slices were oriented orthogonal to the axial slices for each

imaged level.

Following acquisition in the neutral position the subjects were repositioned into left

trunk rotation by the placement of a dense foam cushion wedge under the left

hemipelvis and image sequences repeated (Figure 7.1).

7.3.1 Image analysis

Direction and magnitude of lateral flexion at each level was determined from coronal

T1 weighted MR images in the rotated position by placing a line of best fit across the

superior and inferior vertebral body end-plates of each intervertebral level. Image

Page 121: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 7: The older cohort study

Page VII-4

analysis software (NIH Image-J, Bethesda, USA) was used to measure the lateral

flexion angle.

Figure 7.1: Subject positioning on the gantry of the Magnetic Resonance imager. A

high density foam wedge cushion (arrow) under the left hemipelvis induces left lumbar

rotation

Coronal plane NP deformation was determined from analysis of pixel intensity using a

modification to a previously reported technique (Fazey et al., 2006) and Image-J

software. On each neutral and left rotated mid disc T2 weighted axial image three lines

were placed horizontally from right to left (Figure 7.2A). Raw pixel data from each set

of lines were normalised to 100 points and averaged (Figure 7.2B) within a Labview

routine (National Instruments, Austin, USA).

Segmental rotation angles, Ø, were derived from axial images as the angle subtended at

the intersection of a line extending through the mid disc and interlaminar points and the

horizontal image border (Figure 7.2C). Intersegmental rotation angles were taken as the

difference between the segmental angles of the respective subjacent segments.

Processed data were imported into Excel (Microsoft Corporation, Redmond, USA)

where magnitude and direction of NP deformation were assessed. As movement of the

isolated peak pixel point may not represent general fluid shift, total pixel numbers either

side of the 50th

percentile of the normalised averaged profiles were used to calculate

direction and percentage of NP hydration offset. This offset was derived for the neutral

resting position and compared with that from the rotated position; the difference

expressed as a percentage.

Page 122: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 7: The older cohort study

Page VII-5

Figure 7.2: Pixel numbers are averaged from three samples across the mid disc region

(A) on axial T2 weighted images from which hydration profiles (B) are derived to

calculate direction and extent of NP deformation. Note peak pixel point may not

represent magnitude of entire NP signal shift (B). Segmental rotation measured by the

angle (Ø) subtended between a line through the interlamina region and the centre of the

vertebral body with the image border (C). Subtraction of the derived angle from that of

the level below produced the intersegmental rotation angle (Ø).

Each disc was graded and classified by an experienced MRI radiologist (SS) on a 4

point scale from T2 weighted sagittal images as either: normal, mild, moderate or

severely degenerated. Grade was based upon the presence of osteophytes, disc height,

disc bulging and signal intensity.

All angle based measures demonstrated acceptable repeat reliability over 10 occasions

on a single image with coefficients of variation (CV) of between 1 – 3.7%. CV for NP

deformation percentage was <3%.

7.3.2 Data analysis

Descriptive statistics were used to inspect data recorded for NP deformation direction

and magnitude. Data were also evaluated for any directional relationship between NP

deformation and segmental lateral flexion range using least squares linear regression.

Comparisons were made between intervertebral levels and between subjects. A

probability of p<0.05 was used as the criterion to define meaningful differences.

7.4 Results

The mean NP deformation in the left rotated position across all subjects was 2.1%

(range: 0.1 – 6.3). By gender the mean percentages of NP deformation were 2.4%

(range: 0.1 – 6.3) and 1.8% (range: 0.2 – 4.3) for males and females respectively (Table

7.1).

Page 123: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 7: The older cohort study

Page VII-6

Table 7.1: Percentage NP deformation by intervertebral level

Subject 1

2 3 4 5 6 7 8 9 10 11 mean SD range

Gender F

M M M M F M F M F F

Age 55

46 40 50 48 54 48 46 57 47 41 48.4 5.4 40 – 57

L1-2 *

0.92 2.54 2.27 6.02 1.84 2.56 0.13 1.94 2.78 0.46 1.95 1.64 0.13 – 6.02

L2-3 4.27

4.75 0.23 4.65 1.84 1.35 0.51 1.12 3.69 2.03 3.42 2.53 1.68 0.23 – 4.65

L3-4 0.29

2.63 1.68 2.11 1.58 2.93 0.33 0.82 2.58 3.48 1.63 1.82 1.05 0.29 – 3.48

L4-5 0.17

1.47 0.89 6.35 5.29 3.34 0.5 0.84 0.07 0.84 4.16 2.17 2.22 0.07 – 6.35

L5-S1 1.49

3.88 1.9 3.92 2.75 0.48 1.0 3.53 1.49 2.57 0.38 2.13 1.29 0.38 – 3.92

* Scan series incomplete in this case. Data are degrees (°)

Page 124: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 7: The older cohort study

Page VII-7

Mean NP deformations by level and gender are represented in Figure 7.3. No difference

was noted between levels or genders with the exception of L1-2 where males

demonstrated smaller mean range of NP deformation. Deformation was greater at L2-3.

In the left rotated position the NP deformed towards the left in 26 (47.3%) and to the

right in 29 (52.7%) of discs.

Figure 7.3: Mean NP deformation represented by gender and intervertebral level. A

trend towards greater deformation at L2-3 is noted.

Mean intersegmental lateral flexion and rotation ranges for each intervertebral level are

reported in Table 7.2. In the left rotated position of the 55 segments assessed, segmental

lateral flexion occurred to the left on 32 occasions and to the right on 23 (Table 7.2).

There were no intervertebral level trends for segmental lateral flexion direction apart

from a modest correlation between intersegmental lateral flexion and NP deformation at

L3-4 [r=0.382, p=0.034] (Figure 7.4).

From the pixel profiling in the resting supine position, all cases showed the hydration

offset to be within 10% of the 50th

percentile (mean: 3.37%, range: 0 – 9.8). The NP

hydration offset in the resting position was right of the 50th

percentile of linear IVD

width in 67.3% of cases and to the left in 32.7%.

Page 125: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 7: The older cohort study

Page VII-8

Figure 7.4: A summary of the associations indexed by intervertebral level between

segmental rotation, coincident lateral flexion and NP deformation in the left rotation

position.

Table 7.2: Intersegmental lateral flexion and rotation absolute mean angles and

direction (number of cases) in the left rotated position

Level L1 – 2 L2 – 3 L3 – 4 L4 – 5 L5 – S1

Mean LF° 3.3 3.8 3.7 3.1 2.7

Mean Rot° 1.7 1.8 2.2 2.5 2.5

Left 7 5 5 8 7

Right 4 6 6 3 3

The direction of NP deformation relative to the direction of segmental lateral flexion is

shown in Table 7.2. In total 34/55 (61.8%) deformed to the contralateral side.

The NP deformed to the left more often in males (63.3%) than females (28%). Males

disc NPs also deformed contralaterally more often (70%) than those of female discs

(52%) (Figure 7.5).

Page 126: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 7: The older cohort study

Page VII-9

Figure 7.5: NP deformation relative to direction of segmental lateral flexion by gender

and intervertebral level. Contralateral direction is represented by grey and ipsilateral by

white.

Each level was inspected and graded for degenerative change. Grades of degeneration

and frequency of occurrence by intervertebral level are shown in table 7.3.

Table 7.3: Numbers of cases and grades of degeneration for all intervertebral levels

Level L1-2 L2-3 L3-4 L4-5 L5-S1

Normal 8 8 6 4 0

Mild 2 1 5 5 1

Moderate 1 2 0 2 7

Severe 0 0 0 0 3

Severely degenerated discs only occurred at L5-S1 (2 male; 1 female). Moderate

degeneration was found more frequently at every level except L3-4. No discs at L5-S1

were graded normal. There was no obvious relationship between the grade of

degeneration and percentage NP deformation at individual intervertebral levels. The

mean percentage NP deformation for each grade of degeneration being: normal, 2.17;

mild, 2.36; moderate, 1.94; severe, 2.11.

7.5 Discussion

This study is the first to report the direction and quantify the extent of NP deformation

in lumbar IVDs of older subjects placed in left rotation from the supine position. The

predictability of coronal plane deformation direction relative to rotation was low with

approximately half deforming to either right or left. The hypothesis that larger lateral

Page 127: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 7: The older cohort study

Page VII-10

flexion angles would correspond with increased NP deformation magnitude is not

supported by the present study apart from a modest association at L3-4. The hypothesis

that higher grades of degeneration would reduce the extent of NP deformation is not

supported as similar deformation magnitudes were seen across all grades of

degeneration. Additionally the hypothesis that NP deformation direction would occur

contralateral to the direction of lateral flexion was supported in 61.8% of IVDs.

The extent of NP deformation is less than previously reported in younger female

subjects by approximately 50% (Fazey et al., 2006) although this study employed

combined sagittal and axial plane subject positioning rather than in the isolated axial

plane as in the present study.

Previous reports suggesting reduced predictability of NP deformation behaviour in the

presence of degenerative change focussed only on sagittal plane postures (Brault et al.,

1997; Edmondston et al., 2000). As most studies, including the present, report variable

response and some degree of inconsistency it is reasonable to assume that this is a

common feature. While Edmondston et al (2000) suggested that degenerative change

may contribute to inconsistency that study did not find that such a variation was

exclusive to degenerated IVDs. Other authors have described inconsistent NP

directional behaviour in abnormal discs but did not define degeneration stage (Beattie et

al., 1994; Brault et al., 1997).

As degeneration results in loss of NP load bearing capability and increased anular

loading (Adams et al., 1996) it is likely assumed that this must influence the hydrostatic

properties of the IVD. A number of other factors may contribute: reduced proteoglycan

content, and therefore water holding capacity, is accompanied by increased collagen and

other structural changes (Hadjipavlou et al., 2008). As hydrostatic behaviour is peculiar

to fluids then areas of non fluid structure would be expected to behave differently. As

the degenerated IVD tends to exhibit irregular hydration signal on T2 weighted MR

images (Figure 7.6) it can be hypothesised that only the hydrated areas will behave

hydrostatically. Imaging and subsequent analysis that attempts to characterise behaviour

of the entire IVD may therefore reveal areas that do not behave in such a characteristic

manner.

Distribution of degenerative grades across intervertebral levels was generally as

expected given the inclusion of all lumbar levels and a trend for subject ages towards

the lower end of the reported range.

Page 128: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 7: The older cohort study

Page VII-11

Figure 7.6: Three dimensional representation of hydration profile showing relative

difference in signal strength between normal L4-5 IVD of a 24 year old male (A) and

degenerated L5-S1 IVD of a 48 year old male (B). Note the patchy hydration profile in

B.

Any correlation between NP deformation and lateral flexion range would be expected to

be positive given the normal fluid mechanics of a well hydrated IVD. Deformation of

fluid based compounds within the disc typically occurs from an area of high to low

compression. The expectation that the NP will always deform away from an area of

compressive force does not consider internal pressure gradients. While intradiscal

pressures have been reported they are static and typically derived from pressure

transducer readings in the mid-disc region (Nachemson, 1960; Sato et al., 1999; Wilke

et al., 1999). It may be hypothesised that if unilateral tensile force exceeds compressive

force on the opposite side then net NP deformation would occur towards the side of

compression rather than away. This theory would require an intact anulus and may

explain variations in directional trends of the NP in normal IVDs.

Studies of intradiscal pressure relative to rotation report only compressive force within

the disc (van Deursen et al., 2001; Wilke et al., 1996; Yantzer et al., 2007). In vivo

studies to differentiate tensile and compressive force influences on the IVD would be

technically difficult but may be feasible within a suitable animal model.

Page 129: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 7: The older cohort study

Page VII-12

7.6 Limitations

This study was limited to a sample of 11 subjects. Although each lumbar level was

imaged and analysed for NP deformation patterns, comparison within and between

intervertebral levels a larger sample size may be more revealing of trends.

Gender differences noted in both laterality of NP deformation and direction relative to

both lateral flexion and rotation may be an effect of sample size rather than true gender

differences as these have not been reported relative to IVD geometry (Farfan et al.,

1972).

The non weightbearing, unidirectional subject positioning in the present study restricts

the ability to relate these observations to functional behaviour of the spine.

Averaging data from three samples across each IVD, a more extensive sampling method

than previous reports, (Alexander et al., 2007; Brault et al., 1997; Edmondston et al.,

2000) may still not accurately represent the hydration pattern within the entire IVD.

7.7 Future studies

Farfan reported the influence of disc geometry on the pattern of disc degeneration and

anular tears concluding that disc shape and articular process symmetry were relative

(Farfan et al., 1972). It may be that such geometrical variants also influence NP

deformation patterns through changes in the anular constraint patterns of the NP. While

the original studies were post mortem the advent of multiplanar and three dimensional

imaging using weightbearing MRI would allow such studies to be performed in vivo.

Replication of the present study with larger subject numbers and a cohort of younger

adult subjects would facilitate comparisons.

7.8 Conclusion

Lumbar NP deformation direction in older subjects positioned in left rotation is not

predictable. Deformation direction relative to intersegmental lateral flexion direction

showed a trend towards the contralateral side. No consistent relationship was found

between mean NP deformation and intersegmental lateral flexion angles.

Page 130: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 7: The older cohort study

Page VII-13

References

Adams M, Bogduk N, Burton K, Dolan P. The Biomechanics of Back Pain. London,:

Churchill Livingstone, 2002.

Adams MA, McNally DS, Dolan P. 'Stress' distributions inside intervertebral discs: the

effects of age and degeneration. The Journal of Bone and Joint Surgery Br 1996;

78(6): 965-72.

Adams MA, Stefanakis M, Dolan P. Healing of a painful intervertebral disc should not

be confused with reversing disc degeneration: implications for physical therapies

for discogenic back pain. Clin Biomech (Bristol, Avon) 2010; 25(10): 961-71.

Alexander LA, Hancock E, Agouris I, Smith FW, MacSween A. The response of the

nucleus pulposus of the lumbar intervertebral discs to functionally loaded

positions. Spine 2007; 32(14): 1508-12.

Beattie PF, Brooks W, Rothstein J. Effect of lordosis on the position of the nucleus

pulposus in supine subjects. Spine 1994; 19: 2096-102.

Brault J, Driscoll D, Laakso L, Kappler R, Allin E, Glonek T. Quantification of lumbar

intradiscal deformation during flexion and extension by mathematical analysis

of magnetic resonance imaging pixel intensity profiles. Spine 1997; 22: 2066-

72.

Edmondston S, Song S, Bricknell R, Davies P, Fersum K, Humphries P, Wickendon D,

Singer K. MRI evaluation of lumbar spine flexion and extension in

asymptomatic individuals. Manual Therapy 2000; 5: 158-64.

Farfan HF, Cossette JW, Robertson GH, Wells RV, Kraus H. The effects of torsion on

the lumbar intervertebral joints: the role of torsion in the production of disc

degeneration. J Bone Joint Surg Am 1970; 52(3): 468-97.

Farfan HF, Huberdeau RM, Dubow HI. Lumbar intervertebral disc degeneration: the

influence of geometrical features on the pattern of disc degeneration - a post

mortem study. J Bone Joint Surg Am 1972; 54(3): 492-510.

Fazey P, Song S, Mønsas A, Johansson L, Haukalid T, Price R, Singer K. An MRI

investigation of intervertebral disc deformation in response to torsion. Clinical

Biomechanics 2006; 21: 538-42.

Hadjipavlou AG, Tzermiadianos MN, Bogduk N, Zindrick MR. The pathophysiology of

disc degeneration: a critical review. J Bone Joint Surg Br 2008; 90(10): 1261-70.

Haughton V. Imaging intervertebral disc degeneration. J Bone Joint Surg Am 2006; 88

Suppl 2: 15-20.

Haughton V, Rogers B, Meyerand M, Resnick D. Measuring the axial rotation of

lumbar vertebrae in vivo with MR imaging. American Journal of

Neuroradiology 2002; 23: 1110-6.

Jensen TS, Bendix T, Sorensen JS, Manniche C, Korsholm L, Kjaer P. Characteristics

and natural course of vertebral endplate signal (Modic) changes in the Danish

general population. BMC Musculoskelet Disord 2009; 10: 81.

Jensen TS, Karppinen J, Sorensen JS, Niinimaki J, Leboeuf-Yde C. Vertebral endplate

signal changes (Modic change): a systematic literature review of prevalence and

association with non-specific low back pain. Eur Spine J 2008; 17(11): 1407-22.

Johansen JG, Nork M, Grand F. Torsional instability of the lumbar spine. Rivista di

Neuroradiologia 1999; 12: 193-5.

Luoma K, Vehmas T, Riihimaki H, Raininko R. Disc height and signal intensity of the

nucleus pulposus on magnetic resonance imaging as indicators of lumbar disc

degeneration. Spine 2001; 26(6): 680-6.

Nachemson A. Lumbar intradiscal pressure. Acta Orthopaedica Scandinavica,

Supplementum 1960; 43: 1-104.

Page 131: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 7: The older cohort study

Page VII-14

Salminen JJ, Erkintalo-Tertti MO, Paajanen HE. Magnetic resonance imaging findings

of lumbar spine in the young: correlation with leisure time physical activity,

spinal mobility, and trunk muscle strength in 15-year-old pupils with or without

low-back pain. J Spinal Disord 1993; 6(5): 386-91.

Sato KMDD, Kikuchi SMDD, Yonezawa TMD. In Vivo Intradiscal Pressure

Measurement in Healthy Individuals and in Patients With Ongoing Back

Problems. Spine 1999; 24(23): 2468-74.

van Deursen D, Snijders C, van Dieën J, Kingma I, van Deursen L. The effect of

passive vertebral rotation on pressure in the nucleus pulposus. Journal of

Biomechanics 2001; 34: 405- 8.

Wilke HJ, Neef P, Caimi M, Hoogland T, Claes LE. New in vivo measurements of

pressures in the intervertebral disc in daily life. Spine 1999; 24(8): 755-62.

Wilke HJ, Wolf S, Claes LE, Arand M, Wiesend A. Influence of varying muscle forces

on lumbar intradiscal pressure: an in vitro study. J Biomech 1996; 29(4): 549-

55.

Yantzer BK, Freeman TB, Lee WE, 3rd, Nichols T, Inamasu J, Guiot B, Johnson WM.

Torsion-induced pressure distribution changes in human intervertebral discs: an

in vitro study. Spine 2007; 32(8): 881-4.

Page 132: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

CHAPTER 8

Page VIII-1

The scoliosis cohort MRI study

8.1 Summary

Scoliosis reflects morphological changes to the vertebral elements and compensatory

wedging of the intervertebral bodies and discs with exaggerated axial, sagittal and

coronal spinal alignment. The purpose of this study was to provide a detailed

assessment of the hydration distribution within the nucleus pulposus (NP) of the lumbar

intervertebral disc in scoliosis cases.

Twelve cases of adolescent scoliosis were assessed with MRI as part of a routine pre-

surgical workup. Thoracic and lumbar image sequences were used to derive the Cobb

angle and the apical disc wedge angle. The extent of any coronal plane nucleus

deformation was measured using a hydration profiling technique.

Lumbar Cobb angles ranged from 12.4° to 54.6°, with a mean of 34.9°. Intersegmental

rotation at the apex ranged from 0.8° to 8.0°, with a mean of 4.6°. Segmental lateral

flexion ranged from 4.2° to 13.7°, with a mean of 7.5°. The apical NP showed an offset

away from the midline which was weakly associated with the extent of the Cobb angle

(r=0.12).

Adolescent lumbar compensatory scoliosis results in exaggeration of the three cardinal

planes which coupled with disc wedging contribute to an offset deformation of the NP

away from the compressive axis. In general, the greater the disc wedging and lumbar

Cobb angles the further the displacement of the NP.

Page 133: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 8: The scoliosis study

Page VIII-2

8.2 Introduction

Idiopathic scoliosis affects 2%-3% of children aged between 10 and 16 years (Reamy &

Slakey, 2001) with females representing 90% of cases with Cobb angles >30°. Scoliosis

is a tri-dimensional phenomenon with deformity components involving axial, coronal

and sagittal planes. In 90% of cases the primary curvature convexity is to the right and

where a compensatory lumbar curve exists, a left convexity is found in 70% of cases.

A major focus of the literature concerns the coronal plane deformity, exemplified by the

Cobb angle measurement (Cobb, 1948), with relatively less consideration of the axial

plane component. Fewer studies yet have considered the effect of scoliosis on the

intervertebral disc (IVD) and the extent to which the nucleus pulposus (NP) is deformed

in relation to the magnitude of the secondary lumbar curve. Périé (Périé et al., 2003) has

reported three dimensional mathematical modelling of NP using Magnetic Resonance

Imaging (MRI) in primary thoracic idiopathic scoliosis. Although NP deformation is

reported it is not quantified. Violas (Violas et al., 2007a; b) proposed a similar three

dimensional reconstruction of the NP in secondary lumbar scoliotic curves and

calculated a volume ratio between NP and the entire disc. Although this ratio reflects

relative tissue hydration there was no assessment of variations within the NP. Further,

the extent of NP deformation was not quantified.

Traditional imaging of scoliosis relies upon plain posterior-anterior (PA) radiographs

from which Cobb angles are derived and curve progression can be monitored; an

approach restricting this assessment to two dimensions. Computerised tomography (CT)

and MRI provide an accurate way of imaging the scoliotic spine, resulting in a greater

understanding of the tri-dimensional nature of the condition (Wright, 2000). MRI is

typically used to exclude occult neurological pathology such as hydromyelia,

syringomyelia and tethered cord (Wright, 2000). MRI may also enable characterisation

of NP deformation direction and magnitude as a result of the deformity.

Nucleus pulposus deformation in the lumbar region has been documented using MRI in

healthy cases, relative to subject positioning in the sagittal (Beattie et al., 1994;

Edmondston et al., 2000; Fennell et al., 1996), coronal (Fazey et al., 2010) and axial

planes (Fazey et al., 2006). The consistent trend has been to observe in the majority of

cases, an offset deformation of the NP away from the area of greatest compression. In

sagittal plane flexion the NP adopts a posterior locus; in side flexion a locus to the

Page 134: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 8: The scoliosis study

Page VIII-3

convexity of the posture and, in rotation a mixed position that combines the effect of

axial and side-flexed load upon the intervertebral disc (IVD).

Axial rotation, measured with a variety of two and three dimensional methods (Vrtovec

et al., 2009), provides quantitative information on surgical or conservative management

results (Pinheiro et al., 2009), where correction to a more neutral alignment is the

objective. Axial rotation at the apex of the lumbar curvature can be used to reliably

predict post operative coronal spinal decompensation (Behensky et al., 2007).

Coronal plane deformity is evaluated routinely using the method described by Cobb

and may be applied to both primary thoracic and secondary lumbar curves. A regional

assessment of curvature is achieved in the coronal plane which integrates the effect of

disc and vertebral body wedging. Intersegmental angles which contribute to the

deformity are rarely reported (Wright, 2000).

Axial rotation in scoliosis is an integral component of the deformity and has been

shown to occur in both the IVD and the vertebral body. Up to 55% of axial deformation

in scoliosis has been attributed to torsion of the IVD (Birchall et al., 2005). Wedging

also occurs mainly in the IVD with the vertebral body accorded only 22% of the

asymmetry (Beuerlein et al., 2003). Coupling of axial and coronal plane motion in the

spine occurs physiologically, although these relationships have not been investigated

definitively (Panjabi, 1989). Lateral bending of the scoliotic spine does not induce

coupled axial rotation either in primary thoracic or secondary lumbar curves at the apex

(Beuerlein et al., 2003). No studies to date have considered, in the lumbar region of

scoliotic spines, the association between NP deformation and the degree of

intersegmental coronal plane wedging or intersegmental rotation angle. The purpose of

this MRI study was to quantify NP deformation in secondary lumbar curvature of

subjects with scoliosis and to consider the association between IVD wedge angulation

and NP offset using a method developed specifically for a lumbar spine model.

8.3 Methods

Preoperative magnetic resonance images and plain radiographs were obtained

retrospectively for 14 subjects; 2 male and 12 female, with a mean age of 13.5 years

(range: 12-19).

Subjects were identified by three spinal deformity surgeons (PW, EM and DD) as

potential candidates for corrective surgery and had undergone routine pre-operative

Page 135: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 8: The scoliosis study

Page VIII-4

staging. This included standing plain P-A radiographs for Cobb angle measurement, and

coronal plus axial MRI sequences to exclude occult neurological pathology.

Subject selection criteria included presence of a secondary lumbar curve and availability

of T2 weighted axial MR screening images through the mid-disc region at the apex of

the lumbar curve. Over 100 archived cases were reviewed to determine those where

optimal T2-weighted lumbar images sequences were available for this sub-set

investigation. The most frequent reasons for exclusion were: Complete MRI sequences

unavailable – 55%, T2 weighted axial images through mid disc region unavailable –

35%.

Coronal plain radiographs were used to derive Cobb angles of the lumbar curvature

employing the method described by Cobb (Cobb, 1948) plus Dicom image analysis

software (Philips MxLiteView, Andover, USA). A line was placed along the superior

and inferior vertebral end plates defining the lumbar curve. The angle of intersection of

perpendicular lines subtended from each was recorded as the Cobb measurement.

Intersegmental lateral flexion angulation was measured in the coronal plane from MRI

images using the same image analysis software. Lines were inscribed along adjacent

end plates and the angle, θ, subtended by orthogonal extensions recorded as the

intersegmental lateral flexion angle in degrees (Figure 8.1A).

Segmental axial rotation was defined as the angle, Ø, subtended by the horizontal

image margin and a line drawn through the midpoint of the inter lamina region and the

spinous process (Figure 8.1B). Intersegmental angle was derived by subtracting the

segmental axial rotation of the cranial segment from that of the subjacent level of the

target motion segment. All angle based measures demonstrated acceptable intra-image

repeat reliability over 10 occasions with coefficients of variation of between 1-3.7%.

Direction of NP deformation was derived from the T2 weighted mid-disc axial images

at, plus adjacent to, the apex of the lumbar curve using a previously validated technique

(Fazey et al., 2006) and image analysis software (Image-J, NIH, Bethesda, USA). This

enabled pixel intensity profiling to represent the relative hydration pattern across the

disc. On axial images, 3 closely spaced parallel lines were placed across the mid-disc

region from right to left (Figure 8.2A). Pixel positions along each line were normalised

to 100 points and averaged using a Labview software routine (National Instruments,

Austin, USA) (Figure 8.2B). These data were imported into Excel where the direction

and magnitude of any offset of the NP profile was derived.

Page 136: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 8: The scoliosis study

Page VIII-5

Figure 8.1: Cobb methodology for calculation of segmental coronal plane angulation

(A). Segmental rotation (B) was measured by the angle subtended between a line

through the interlamina region and the centre of the vertebral body with the image

border. Subtraction of the result from that of the level below gives the intersegmental

rotation angle incorporating the target IVD.

Figure 8.2: NP deformation was measured from the mean pixel intensity of three lines

placed across the mid disc region of the apical IVD (A). These data were plotted and

averaged (B) to calculate NP hydration offset.

Descriptive statistics were used to report all data and linear regression used to inspect

relationships between direction and magnitude of NP deformation and intersegmental

lateral flexion and Cobb angles. A probability of p<0.05 defined a meaningful statistical

association.

Page 137: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 8: The scoliosis study

Page VIII-6

8.4 Results

As there was no gender difference in the NP deformation data, the cases were pooled for

all analyses. Results for intersegmental lateral flexion angles, inter segmental axial

rotation angles, NP deformation extent and lumbar Cobb angles, are shown in table 8.1.

The apical level varied between subjects, occurring most commonly at L2-3 (50%) with

T12-L1 the next most common (28%). In two cases the apex occurred at L1-2. In all

cases the NP deformed towards the convexity of the lumbar curve and away from the

intersegmental lateral flexion direction. Segmental axial rotation occurred in the same

direction as the concavity in all cases. Mean NP deformation was 17.5% (range: 0.6 –

58.7).

A weak relationship (r=0.1) was seen between lateral flexion segmental angulation

range and NP deformation magnitude. Similarly there was no relationship between

either NP deformation and lumbar cobb angles, or between NP deformation and

segmental rotation angles.

Table 8.1: Lumbar mobility and nucleus pulposus deformation in apical segments of

secondary lumbar curve of 14 subjects with scoliosis.

Mean SD Range

Lateral Flexion (°) 7.5 2.4 4.2 – 13.7

Segmental Rotation (°) 4.6 2.1 0.8 – 8.0

NP deformation (%) 17.5 13.8 0.6 – 58.7

Cobb (°) 34.9 13.7 12.4 – 54.6

Figure 8.3: Two dimensional coronal (A) and axial (B) T2 weighted magnetic

resonance images show hydration signal offset away from the concavity. The three

dimensional representation (C) highlights the offset and variation across the entire IVD.

8.5 Discussion

This study sought to quantify NP deformation relative to segmental axial rotation and

coronal plane angulation at the apex of secondary lumbar curvature in 14 adolescent

scoliosis cases.

A B C

Page 138: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 8: The scoliosis study

Page VIII-7

As expected, the results showed an association between the direction of NP deformation

and the direction of both the regional and segmental lateral flexion, with all NPs

deforming contralaterally and towards the convexity. While such a directional

relationship was anticipated given the hydrostatic nature of NP mechanics and

propensity for fluid shift away from offset compressive loading this has not always been

demonstrated. A previous study revealing a similar trend in normal subjects reported a

few cases (5%) where NP deformed towards the concavity (Fazey et al., 2010). This

tended to occur at non apical segments having smaller ranges of lateral flexion. The

stronger relationship in the present study may be attributable to generally larger ranges

of lateral flexion, particularly at the apical segments, and the effects of longstanding

structural deformity.

Structural and histochemical changes have been demonstrated specific to either the

convexity or concavity within the IVD. Consistent with the observed deformation,

Roberts et al (1993) reported reduced proteoglycan and water content in both the end-

plate and IVD, particularly on the concave side in scoliosis. While readily attributable to

offset compressive loading, such histochemical changes are also postulated to be

associated with curve progression (Roberts et al., 1993). Additionally, significantly

higher levels of collagen cross linking within the IVD on the convex side along with

increased metalloproteinases are presumed to represent increased matrix turnover and

tissue remodelling (Crean et al., 1997; Duance et al., 1998). It is unclear whether these

changes associated with deformity towards convexity are causative or a result of the

deformity.

There were only weak relationships between the magnitude of NP deformation and that

of the regional Cobb or segmental lateral flexion angles. While it could be reasonably

assumed that the magnitude of offset loading characterised by Cobb and/or segmental

lateral flexion angles relative to that of NP deformation would be predictable this has

never been reported. This weak relationship may be explained by the end range nature

of the deformity. Within an intact anulus the NP is constrained by the capsular function

of the inner anular fibres, when those on the convex side reach maximum tension no

further NP deformation towards that side is possible. Further small movements into

lateral flexion will gain increased segmental angulation due to fibre creep but still not

permit further deformation. On this basis a stronger relationship may be evident within

sub maximal lateral flexion ranges. It could also be postulated that if the tensile forces

in the anular fibres at the convexity exceed the compressive force then NP deformation

Page 139: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 8: The scoliosis study

Page VIII-8

could be ipsilateral to the offset compressive load. This observation has previously been

reported in a minority of subjects (Fazey et al., 2010).

There was no relationship between NP deformation magnitude and segmental rotation

angles. The related literature reports a directional relationship between NP deformation

and rotation but does not report its strength (Fazey et al., 2006). A stronger relationship

with between NP deformation and lateral flexion in normal subjects is postulated (Fazey

et al., 2006). The present study showed a strong directional relationship between

rotation and NP deformation direction but this is likely attributable to the consistent

ipsilateral direction of axial rotation and lateral flexion in scoliosis.

Though intersegmental rotation angles were small they were greater than those

previously reported in asymptomatic volunteers (Haughton et al., 2002; Pearcy &

Tibrewal, 1984). While these studies report intervertebral angles, results of the present

study may reflect additional rotary deformity within the vertebral body as well as the

IVD (Birchall et al., 2005). Subject positioning within the MRI may influence rotation

range. It is reported that supine positioning relaxes sagittal and coronal curves and

presumably axial rotation (Birchall et al., 1997; Torell et al., 1985) though this is

disputed (Ho et al., 1993). Future studies using a standing open magnet MRI would help

resolve the question.

The weak negative relationship between rotation and lateral flexion angles may suggest

greater ranges of rotation are possible in the presence of less lateral flexion. This is

consistent with the biomechanical principle that primary motion in one plane influences

available range in a subsequent plane (Pearcy & Hindle, 1991; White & Panjabi, 1990)

though this has not been reported relative to structural changes in scoliosis (Birchall et

al., 2005; Liljenqvist et al., 2002).

Previous studies measuring NP deformation have sought to quantify excursion of fluid

shifts by comparing measurements from a neutral starting position with those from a

subsequent posture, either flexion, rotation or lateral flexion (Edmondston et al., 2000;

Fazey et al., 2006; Fazey et al., 2010). In this study subjects were imaged in the resting

position only; therefore no quantification of further passive rotation was possible.

Resting position of the NP was assessed relative to the linear mid-position of lines

across the disc (Figure 8.2). This position is somewhat arbitrary as a truly neutral

positioning of the NP at rest would be rare (Fazey et al., 2010).

Scoliosis is frequently imaged with conventional plain radiographs in both the resting

and traction position to assess the degree of correction and potential management

Page 140: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 8: The scoliosis study

Page VIII-9

options. It would be of interest for future studies employing the same MRI

methodology to measure NP deformation in both resting and traction positions to

determine the relationship between magnitude of change in the two imaged positions.

This could be done both immediately and over time to test the ability of this

methodology to predict correction.

T2 weighted MRI is an elegant choice of modality to elucidate hydration profiles from

pixel intensity (Boos et al., 1994). Three dimensional image analysis would be optimal

for this purpose to elaborate the detail of hydration profiles (Figure 8.3).

Quantification of NP deformation in the lumbar curvature may also predict post

operative outcome or provide a reliable method to assess outcomes following

conservative management.

8.6 Limitations

This study was limited to a small number of subjects with idiopathic scoliosis of

sufficient magnitude to contemplate surgical intervention. Future studies should include

cases with lesser degrees of curvature and extend to other vertebral levels including the

primary thoracic curve. Positioning is known to influence curve size, therefore a

comparison with weightbearing in a standing MR imager would clarify the degree to

which position influences NP deformation. Comparisons between the methodology used

in the present study and three dimensional image analysis of the entire disc would

further elaborate the utility of such a method. The use of various disparate methods of

segmental rotation measurement applied to images may devalue comparisons with

reported ranges in the literature (Cassar-Pullicino & Eisenstein, 2002).

8.7 Conclusions

This study in subjects with idiopathic scoliosis has demonstrated that NP deforms

towards the side of convexity in the apex of secondary lumbar curves in a highly

predictable way. There was weak correlation between the degree of deformation and

segmental lateral flexion angulation or Cobb angle. No relationship was demonstrated

between NP deformation and intersegmental rotation angles.

Page 141: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 8: The scoliosis study

Page VIII-10

References

Beattie PF, Brooks W, Rothstein J. Effect of lordosis on the position of the nucleus

pulposus in supine subjects. Spine 1994; 19: 2096-102.

Behensky H, Cole AA, Freeman BJ, Grevitt MP, Mehdian HS, Webb JK. Fixed lumbar

apical vertebral rotation predicts spinal decompensation in Lenke type 3C

adolescent idiopathic scoliosis after selective posterior thoracic correction and

fusion. Eur Spine J 2007; 16(10): 1570-8.

Beuerlein MJ, Raso VJ, Hill DL, Moreau MJ, Mahood JK. Changes in alignment of the

scoliotic spine in response to lateral bending. Spine 2003; 28(7): 693-8.

Birchall D, Hughes D, Gregson B, Williamson B. Demonstration of vertebral and disc

mechanical torsion in adolescent idiopathic scoliosis using three-dimensional

MR imaging. Eur Spine J 2005; 14(2): 123-9.

Birchall D, Hughes DG, Hindle J, Robinson L, Williamson JB. Measurement of

vertebral rotation in adolescent idiopathic scoliosis using three-dimensional

magnetic resonance imaging. Spine 1997; 22(20): 2403-7.

Boos N, Wallin A, Schmucker T, Aebi M, Boesch C. Quantitative MR imaging of

lumbar intervertebral disc and vertebral bodies: methodology, reproducibility,

and preliminary results. Magn Reson Imaging 1994; 12(4): 577-87.

Cassar-Pullicino VN, Eisenstein SM. Imaging in scoliosis: what, why and how? Clin

Radiol 2002; 57(7): 543-62.

Cobb J. Outline for the study of scoliosis. American Academy of Orthopaedic Surgeons.

Instructional Course Lectures 1948; 5: 261-75.

Crean JK, Roberts S, Jaffray DC, Eisenstein SM, Duance VC. Matrix

metalloproteinases in the human intervertebral disc: role in disc degeneration

and scoliosis. Spine 1997; 22(24): 2877-84.

Duance VC, Crean JK, Sims TJ, Avery N, Smith S, Menage J, Eisenstein SM, Roberts

S. Changes in collagen cross-linking in degenerative disc disease and scoliosis.

Spine 1998; 23(23): 2545-51.

Edmondston S, Song S, Bricknell R, Davies P, Fersum K, Humphries P, Wickendon D,

Singer K. MRI evaluation of lumbar spine flexion and extension in

asymptomatic individuals. Manual Therapy 2000; 5: 158-64.

Fazey P, Song S, Mønsas A, Johansson L, Haukalid T, Price R, Singer K. An MRI

investigation of intervertebral disc deformation in response to torsion. Clinical

Biomechanics 2006; 21: 538-42.

Fazey PJ, Takasaki H, Singer KP. Nucleus pulposus deformation in response to lumbar

spine lateral flexion: an in vivo MRI investigation. Eur Spine J 2010; 19(7):

1115-20.

Fennell A, Jones A, Hukins D. Migration of the nucleus pulposus within the

intervertebral disc during flexion and extension of the spine. Spine 1996; 21:

2753- 7.

Haughton V, Rogers B, Meyerand M, Resnick D. Measuring the axial rotation of

lumbar vertebrae in vivo with MR imaging. American Journal of

Neuroradiology 2002; 23: 1110-6.

Ho EK, Upadhyay SS, Chan FL, Hsu LC, Leong JC. New methods of measuring

vertebral rotation from computed tomographic scans. An intraobserver and

interobserver study on girls with scoliosis. Spine 1993; 18(9): 1173-7.

Liljenqvist UR, Allkemper T, Hackenberg L, Link TM, Steinbeck J, Halm HF. Analysis

of vertebral morphology in idiopathic scoliosis with use of magnetic resonance

imaging and multiplanar reconstruction. J Bone Joint Surg Am 2002; 84-A(3):

359-68.

Page 142: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 8: The scoliosis study

Page VIII-11

Panjabi M. How does posture affect coupling in the lumbar spine? Spine 1989; 14:

1002-11.

Pearcy M, Tibrewal S. Axial rotation and lateral bending in the normal lumbar spine

measured by three-dimensional radiography. Spine 1984; 9: 582-87.

Pearcy MJ, Hindle RJ. Axial rotation of lumbar intervertebral joints in forward flexion.

Proc Inst Mech Eng [H] 1991; 205(4): 205-9.

Périé D, Curnier D, de Gauzy JS. Correlation between nucleus zone migration within

scoliotic intervertebral discs and mechanical properties distribution within

scoliotic vertebrae. Magn Reson Imaging 2003; 21(9): 949-53.

Pinheiro AP, Tanure MC, Oliveira AS. Validity and reliability of a computer method to

estimate vertebral axial rotation from digital radiographs. Eur Spine J 2009.

Reamy BV, Slakey JB. Adolescent idiopathic scoliosis: review and current concepts.

Am Fam Physician 2001; 64(1): 111-6.

Roberts S, Menage J, Eisenstein SM. The cartilage end-plate and intervertebral disc in

scoliosis: calcification and other sequelae. J Orthop Res 1993; 11(5): 747-57.

Torell G, Nachemson A, Haderspeck-Grib K, Schultz A. Standing and supine Cobb

measures in girls with idiopathic scoliosis. Spine 1985; 10(5): 425-7.

Violas P, Estivalezes E, Briot J, Sales de Gauzy J, Swider P. Objective quantification of

intervertebral disc volume properties using MRI in idiopathic scoliosis surgery.

Magn Reson Imaging 2007a; 25(3): 386-91.

Violas P, Estivalezes E, Briot J, Sales de Gauzy J, Swider P. Quantification of

intervertebral disc volume properties below spine fusion, using magnetic

resonance imaging, in adolescent idiopathic scoliosis surgery. Spine 2007b;

32(15): E405-12.

Vrtovec T, Pernus F, Likar B. A review of methods for quantitative evaluation of spinal

curvature. Eur Spine J 2009; 18(5): 593-607.

White A, Panjabi M. Clinical Biomechanics of the Spine, 2 ed. Philadelphia: Lippincott,

1990;

Wright N. Imaging in scoliosis. Arch Dis Child 2000; 82(1): 38-40.

Page 143: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

CHAPTER 9

Page IX-1

The longitudinal case study

9.1 Summary

Rotation is a frequent mechanism by which the lumbar intervertebral disc (IVD) may be

injured resulting in herniation of the nucleus pulposus.

Conservative management of acute nucleus pulposus herniation is a common option and

produces comparable results to surgery. While there are numerous reports of

spontaneous resorption of extruded nuclear material few studies examine changes over

the longer term or report variables other than protrusion size.

A 32 year old woman with a large central herniated nucleus pulposus at L4-5 was

followed over a 12 year period with serial MRI from which thecal sac dimension, cross

sectional area and percentage fat infiltration of multifidus at L4-5 and L3-4 levels were

derived.

Antero-posterior (A-P) thecal sac dimension was restored as herniation size reduced.

The largest reduction occurring during the initial six months post injury. Cross sectional

area (CSA) of multifidus reduced bilaterally post injury and gradually recovered over

the length of the study period. Fat infiltration markedly increased bilaterally in the

initial six months and gradually reduced over the 12 year period to less than immediate

post injury values.

The natural history of a case of herniated nucleus pulposus demonstrated marked and

continued improvement in herniation size, fat infiltration, cross sectional area of

adjacent muscle and self reported functional capacity over 12 years.

Page 144: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 9: The longitudinal case study

Page IX-2

9.2 Introduction

Intervertebral disc (IVD) injury resulting in herniation of the nucleus pulposus (HNP) is

a common cause of low back pain (Adams et al., 2002). Incidence is increased in the

younger population (Kim et al., 2009) and has been associated with repetitive flexion

(Scannell et al., 2009) and rotational forces (Farfan et al., 1970). Local and/or distal

symptoms are a common sequel with or without altered peripheral neurological status.

Management has traditionally involved surgical options including microdiscectomy

however conservative management has increased in popularity and is reported to have at

least equal outcomes to surgery (Atlas et al., 2005; Singer et al., 2004). Choice of

management approach is often based on lifestyle and patient preference.

The natural course of herniated IVD is for regression of the degree of disc material

protrusion (Benoist, 2002; Cribb et al., 2007; Kobayashi et al., 2003), which has been

postulated to be due in part to resorption and shrinkage of the extruded material

following a complex process of neovascularisation, phagocytosis and immune response

(Autio et al., 2006; Benoist, 2002; Cribb et al., 2007). Numerous reports exist,

predominantly as case studies, of spontaneous resorption of HNP (Kobayashi et al.,

2003) and focus primarily on functional outcomes, symptoms and imaging changes in

the short to intermediate period after injury.

Few studies of HNP give consideration to the effect of injury on adjacent paraspinal

musculature with respect to changes relative to disc injury and the natural history of the

condition. Cross sectional area (CSA) and muscle morphology have been associated

with functional decline and can predispose to recurrence or ongoing symptoms (Hides

et al., 1996). Several authors have reported the CSA of various spinal muscles and their

changes over time relative to symptoms (Barker et al., 2004; Danneels et al., 2000;

Hides et al., 2008) using a variety of imaging techniques including MRI and

ultrasonography .

Acute and late change in muscle morphology, specifically infiltration by fatty tissue,

has been reportedly associated with spinal pain syndromes (Kjaer et al., 2007;

Mengiardi et al., 2006). A cause and effect relationship between fat infiltration and

dysfunction has not been established although it appears to affect the posterior

musculature while sparing anterior structures (Elliott et al., 2008).

In this report we describe the case of a 32 year old female who sustained a large central

L4-5 HNP and elected conservative management. Serial MRI scans over 12 years are

Page 145: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 9: The longitudinal case study

Page IX-3

presented along with evaluation of changes in CSA and fat infiltration of surrounding

musculature.

9.3 Case report

The patient presented with acute onset of low back pain with radiation to the left

buttock, posterior thigh and lateral leg to the ankle. Symptoms were precipitated by

repetitive bending, lifting and twisting while unloading 25kg boxes in a confined space.

On physical examination at three weeks following symptom onset, the patient reported

intolerance to sitting and frequent disturbance of sleep. Erect standing demonstrated a

trunk list to the right. All spinal movements were markedly restricted by pain. Forward

flexion was limited to fingertips reaching above the knees. Extension was <50%. In

supine lying there was marked restriction of Straight Leg Raise (SLR) bilaterally (45°),

with positive cross-over. Light touch sensation was impaired over the L5 distribution in

the posterolateral leg. Deep tendon reflexes were diminished at the patella and absent at

the achilles bilaterally. Lower limb perfusion was normal.

Plain radiographs demonstrated preexistent anterior osteophytes and loss of disc height

at L4-5. Computerised tomography at one week post injury revealed a large

posterocentral disc protrusion. The bony canal dimensions and adjacent disc levels were

normal. At four weeks post onset, lumbar MRI sequences confirmed the extent of the

herniation with migration of disc material inferior to the L5 superior end plate, causing

compression of the ventral aspect of the thecal sac (Figures 9.1A and 9.2). At this time

the patient received left epidural steroid injection at L4-5 under radiological guidance,

resulting in marked improvement in back and leg pain.

On review at eight weeks post injury, SLR remained at 45° left and 60° right. Standing

posture was normal. Following discussion the patient maintained a preference to

continue conservative management including physical therapy, hydrotherapy and anti-

inflammatory medications as required. Following initial improvement in symptoms for

three weeks, a recurrence of radicular symptoms and sleep disturbance necessitated a

second L4-5 epidural at 9 weeks resulting in significant symptom reduction. At this

time forward flexion was still limited by pain to fingertips reaching the knees; while

trunk extension was reduced to approximately 75% of the expected range for her age.

SLR increased to 60° on the left.

Page 146: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 9: The longitudinal case study

Page IX-4

A third epidural was administered at eight months following increased symptoms, again

with good symptomatic effect. Repeat MRI examination at six months demonstrated

marked reduction in the size of the central disc prolapse (Figures 9.1B and 9.2).

Figure 9.1: L4-5 axial T2(A) and T1(B) weighted images acquired in, from left to right,

1997, 1998, 2002 and 2009. Note marked reduction in central disc protrusion between

images taken in July 1997 and January 1998 – a period of six months, and gradual

resorption and reduction in subsequent images.

Figure 9.2: Serial sagittal T2 weighted images acquired, from left to right, in

1997,1998, 2002 and 2009 demonstrating encroachment of extruded disc material into

the spinal canal indenting the thecal sac. Early degenerative change is seen in L4-5 disc,

more marked in the image from 2009.

Page 147: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 9: The longitudinal case study

Page IX-5

On review at 12 months following the injury near normal trunk extension was achieved

and forward flexion enabled fingertips to reach the mid tibia. SLR was now

approximately 75° bilaterally. Subtle reduction in light touch sensation persisted over

the lateral aspect of the left leg.

Repeated MRI at 4.5 years demonstrated further reduction in the extent of the L4-5 disc

herniation since the six month assessment (Figures 9.1 & 9.2). Mild reduction in light

touch sensation persisted. Spinal mobility was slightly limited although movements

were pain free. Symptoms had reduced markedly with report of only occasional activity

related low back pain, in parallel with resumption of normal activity levels.

At the 12 year follow up the patient described minor intermittent left lumbar and

posterior thigh pain associated with sustained sitting. There had been further recent

reduction in these residual symptoms following commencement of regular walking. On

physical examination there was a good range of lumbar active movement with only

slight reproduction of left lumbosacral pain at end range extension. There were no reflex

or power changes and only slight reduction to light touch sensation over the lateral left

lower leg. Straight leg raising was unremarkable and asymptomatic at 85° bilaterally.

MRI on this occasion revealed visible minor residual disc material extending into the

spinal canal but no indentation of the thecal sac. Additionally moderate disc

degeneration was noted at L4-5 with reduction in disc height, end plate irregularity and

osteophytosis. While some degree of degenerative change was noted in 1997 this had

progressed from mild to moderate in the ensuing period.

Retrospective analysis of serial axial T2 weighted images were quantified for thecal sac

A-P dimensions and cross sectional area of multifidus using image analysis software

(NIH Image-J, Bethesda, USA) (Figure 9.3). Fat infiltration of multifidus was measured

using the same image analysis software. Histograms of pixel values were generated of a

region of interest within both muscle and subcutaneous fat from which the percentage of

fat and muscle within the multifidus region (Figure 9.3) was calculated (Table 9.1).

Page 148: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 9: The longitudinal case study

Page IX-6

Figure 9.3: Axial image showing method used to derive linear (A) and area (B)

measurements of thecal sac and multifidus area respectively. Histograms depict pixel

values from muscle (C) and subcutaneous fat (D) and multifidus area (E).

Table 9.1: Summary of results of thecal sac A-P measurements, multifidus cross

sectional area and fat infiltration.

Year Intervertebral

Level

Thecal

sac A-P

(mm)

Multifidus CSA (mm) Fat infiltration (%)

Right Left Right Left

1997 L3-4 14.98 871.77 867.11 39.2 33.46

L4-5 9.4 1058.1 1081.38 34.42 32.02

1998 L3-4 16.58 798.57 696.38 67.51 60.6

L4-5 15.2 922.6 900.72 76.66 53.35

2002 L3-4 16.67 713.18 659.02 37.96 40.63

L4-5 13.33 874.81 821.13 41.61 47.24

2009 L3-4 15.88 855.14 837.79 24.64 17.93

L4-5 14.8 1040.84 1001.34 20.02 26.32

9.4 Discussion

This case follows the natural history over 12 years of symptoms and MRI changes in a

case of conservatively managed HNP. Few reports in the literature span a period of this

duration. It is clear that the greatest reduction in herniation size, as represented by thecal

sac A-P dimension, occurred in the initial six month period with continued reduction

over the remainder of the observation period.

Cross sectional area of the multifidus region was reduced bilaterally at both the level of

injury and the level above. This was a steady reduction over five years following which

there was recovery to almost initial levels. Previous studies have reported that atrophy is

level and side specific and does not spontaneously recover (Hides et al., 1996; Hides et

al., 1994). The results of our case study do not support this conclusion. It may be

Page 149: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 9: The longitudinal case study

Page IX-7

hypothesised that the presence of bilateral lumbar symptoms or the polysegmental

nature of some fascicles of multifidus may have contributed to this variation. The

profound initial atrophy seen may in part result from modification of the patient’s

occupation and functional activities to accommodate the requirement for more

conservative spinal loading during the post-injury period. As the patient did not

undertake a formal exercise program aimed at specific muscle retraining, any changes

identified would be attributable to general activity.

Fat infiltration in the same muscle group showed an initial increase followed by a

decrease over ensuing years. Changes were bilateral and demonstrated at adjacent

levels. Fat infiltration has been postulated to result from either disuse atrophy or

denervation (Elliott et al., 2008) but no conclusive evidence exists to explain its cause.

It is noteworthy that the observed morphological change demonstrated reversal by 12

years post injury. This may be an effect of increased physical activity over the last 18

months during which the patient commenced regular walking exercise.

9.5 Conclusion

This case illustrates conservative management of HNP. Spontaneous resorption of

extruded nucleus pulposus occurs mainly in the first six months but continues gradually

over years. Changes to muscle cross sectional area and fat infiltration may occur at

several levels and may reverse even many years post injury.

Page 150: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 9: The longitudinal case study

Page IX-8

9.6 References

Adams M, Bogduk N, Burton K, Dolan P. The Biomechanics of Back Pain. London,:

Churchill Livingstone, 2002.

Atlas SJ, Keller RB, Wu YA, Deyo RA, Singer DE. Long-term outcomes of surgical

and nonsurgical management of sciatica secondary to a lumbar disc herniation:

10 year results from the maine lumbar spine study. Spine 2005; 30(8): 927-35.

Autio RA, Karppinen J, Niinimaki J, Ojala R, Kurunlahti M, Haapea M, Vanharanta H,

Tervonen O. Determinants of spontaneous resorption of intervertebral disc

herniations. Spine 2006; 31(11): 1247-52.

Barker KL, Shamley DR, Jackson D. Changes in the cross-sectional area of multifidus

and psoas in patients with unilateral back pain: the relationship to pain and

disability. Spine 2004; 29(22): E515-9.

Benoist M. The natural history of lumbar disc herniation and radiculopathy. Joint Bone

Spine 2002; 69(2): 155-60.

Cribb GL, Jaffray DC, Cassar-Pullicino VN. Observations on the natural history of

massive lumbar disc herniation. J Bone Joint Surg Br 2007; 89(6): 782-4.

Danneels LA, Vanderstraeten GG, Cambier DC, Witvrouw EE, De Cuyper HJ. CT

imaging of trunk muscles in chronic low back pain patients and healthy control

subjects. Eur Spine J 2000; 9(4): 266-72.

Elliott J, Sterling M, Noteboom JT, Darnell R, Galloway G, Jull G. Fatty infiltrate in the

cervical extensor muscles is not a feature of chronic, insidious-onset neck pain.

Clin Radiol 2008; 63(6): 681-7.

Farfan HF, Cossette JW, Robertson GH, Wells RV, Kraus H. The effects of torsion on

the lumbar intervertebral joints: the role of torsion in the production of disc

degeneration. J Bone Joint Surg Am 1970; 52(3): 468-97.

Hides JA, Gilmorea C, Stanton W, Bohlscheida E. Multifidus size and symmetry among

chronic LBP and healthy asymptomatic subjects. Manual Therapy 2008; 13: 43-

9.

Hides JA, Richardson CA, Jull GA. Multifidus muscle recovery is not automatic after

resolution of acute, first-episode low back pain. Spine 1996; 21(23): 2763-9.

Hides JA, Stokes MJ, Saide M, Jull GA, Cooper DH. Evidence of lumbar multifidus

muscle wasting ipsilateral to symptoms in patients with acute/subacute low back

pain. Spine 1994; 19(2): 165-72.

Kim MS, Park KW, Hwang C, Lee YK, Koo KH, Chang BS, Lee CK, Lee DH.

Recurrence rate of lumbar disc herniation after open discectomy in active young

men. Spine 2009; 34(1): 24-9.

Kjaer P, Bendix T, Sorensen JS, Korsholm L, Leboeuf-Yde C. Are MRI-defined fat

infiltrations in the multifidus muscles associated with low back pain? BMC Med

2007; 5: 2.

Kobayashi N, Asamoto S, Doi H, Ikeda Y, Matusmoto K. Spontaneous regression of

herniated cervical disc. Spine J 2003; 3(2): 171-3.

Mengiardi B, Schmid MR, Boos N, Pfirrmann CW, Brunner F, Elfering A, Hodler J. Fat

content of lumbar paraspinal muscles in patients with chronic low back pain and

in asymptomatic volunteers: quantification with MR spectroscopy. Radiology

2006; 240(3): 786-92.

Scannell JP, McGill SM. Disc prolapse: evidence of reversal with repeated extension.

Spine 2009; 34(4): 344-50.

Singer KP, Fazey PJ. Disc herniation - non operative treatment. In: Herkowitiz HK,

Dvorak J, Bell G, Nordin M, Grob D editors, The Lumbar Spine, Philadelphia:

Lippincott Williams and Wilkins, 2004.

Page 151: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

CHAPTER 10

Page X-1

Discussion

10.1 Introduction

Over the last century the focus in the spine literature concerning functional mechanics

has been primarily on sagittal plane and less on coronal and axial plane motion. The

purpose of this thesis was to elaborate the functional and mechanical significance of

rotation as it relates to NP deformation.

Several questions naturally arise from this; what is normal, what is abnormal? What is

the effect of age, deformity or injury? Can NP deformation be used to predict the degree

of deformity in scoliosis? Arising from these questions are several themes which will be

expanded in this chapter.

1. Fundamental normal mechanics of NP deformation relative to position.

2. The effect of age and deformity on NP deformation magnitude and predictability

of direction.

3. Differences between the normal and the abnormal.

10.2 Thesis evolution

Chapter 4 of this thesis investigated the effect on rotation range of common

morphological variations involving both facet joints and the IVD. An increase in

available intersegmental range of axial rotation was reported in the presence of IVD

degeneration. This result was consistent with other reports in the literature (Haughton et

al., 2002; Johansen et al., 1999; Singer et al., 2001). As the degenerative process

involves reduction in proteoglycan and therefore water content in the IVD, particularly

the NP, the converse question was raised; what is the mechanical effect of axial rotation

on the hydrostatic mechanism of the lumbar NP?

Appendix 4 documents and approach to examine this question using a novel pixel

profiling method and T2 weighted MRI sequences in young normal subjects. While a

directional bias in NP deformation was seen, the small number of subjects dictated that

a larger cohort be examined with this method and consequently this is reported in

chapter 5.

Page 152: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 10: Discussion

Page X-2

As early results indicated limited predictability of NP deformation in response to axial

rotation position it was hypothesised that conjunct coronal plane motion may have a

more predictable influence. This is postulated in Appendix 4 and chapter 5, and tested

in chapter 6 with application of a refined method to a cohort of young normal subjects

positioned in lumbar lateral flexion.

The natural progression from normal subjects was to extend the method and hypothesis

to age related and spinal deformity cases. Chapter 7 repeats the protocol examining NP

deformation following axial rotation in an older population, some of whom exhibited

age-related degenerative IVD change. Chapter 8 focuses on subjects with idiopathic

scoliosis, a structural pathology involving deformity in both axial and coronal planes.

Rotary injury to the IVD is common and may result in interruption to the internal IVD

environment. Chapter 9 examines this via detailed analysis of a single case of IVD

herniation over 12 years, and also extends to consider concomitant perispinal tissue

effects of chronic pain and disuse atrophy. A single case study reporting rotational

injury and fracture patterns in the presence of skeletal pathology is presented in

Appendix 10.

The effect of axial rotation on predictability of NP deformation has not previously been

reported. Such an examination of the question through the progression described above

contributes an original insight to the literature.

10.2.1 Terminology

Earlier studies, and those of Appendix 4, use the term ‘migration’ when describing

observed changes in NP signal. While there have been reported assessments of this

linear change relative to AF boundaries using a variety of methods (Alexander et al.,

2007; Beattie et al., 1994; Fennell et al., 1996) conclusions cannot be drawn as to

changes in fluid distribution within the NP from such an assessment. Intact inner anular

fibres will constrain NP migration thereby limiting the value of assessments of

magnitude (Figure 10.1). These observations lead to a change in terminology from

chapter 5 to NP ‘deformation’ which was considered more conceptually accurate and

indicative of the variables being tested.

Page 153: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 10: Discussion

Page X-3

Figure 10.1: Schematic representation to propose that intact inner anular fibres limit migration of NP boundaries but allow internal hydration redistribution to attenuate load. (Adapted from Kramer, 1981).

10.3 Theme one – what is normal?

There is an extensive literature reporting normal reference ranges for lumbar motion in

the three cardinal planes (White & Panjabi, 1990). Less information is available for

lateral flexion and axial rotation of the lumbar segments; the main emphasis has been

due to the relative simplicity of measurement of sagittal ranges. The advent of cross

sectional imaging and multiplanar formatting has enabled more detailed insights into

other planar motion and indeed coupled motion. This section details the main insights

made with respect to the derived data from MRI sequences performed using different

cohorts of subjects.

10.3.1 Rotation range

Normal lumbar segmental rotation ranges measured with a variety of methods are

reported in the literature and discussed in chapter 2. Chapter 6 reports rotation ranges in

young asymptomatic subjects but only as a secondary response to primary positioning

into lateral flexion. Consequently they are smaller in magnitude than in reports where

axial rotation is the primary focus either in vivo or ex vivo.

10.3.2 Lateral flexion range

Chapter 6 focuses on lumbar lateral flexion in normal subjects and reports

intersegmental angles. These are greater at the apex, typically L2-3 or L3-4, and least at

the junctional zones. These ranges are smaller than those reported in the literature

(Pearcy & Tibrewal, 1984) possibly reflecting the difference between imaging

modalities or supine versus erect subject positioning.

Page 154: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 10: Discussion

Page X-4

10.3.3 NP deformation

The studies reported in Appendix 4 and chapter 5 quantify lumbar NP deformation

following axial rotation positioning. Chapter 6 does so following lumbar lateral flexion

positioning. In the absence of pre-existing data in the literature, these studies establish

preliminary normal values with respect to magnitude and direction.

10.3.3.1 Direction of NP deformation

The hydrostatic nature of NP mechanics is well established. The hydrated NP will

deform away from compressive load (Keyes & Compere, 1932). The direction of

deformation may then indicate the impact of net compressive load direction. In complex

spinal motion that involves multiplanar coincident motion (White & Panjabi, 1990) it

would be reasonable to infer that the greater load vector will dictate the overall direction

of NP deformation.

Strong directional bias has been reported in sagittal plane positioning in Appendix 4,

this was also found in coronal plane positioning as reported in the lateral flexion cohort

MRI study (chapter 6). This trend is consistent with the literature on this topic in the

sagittal plane (Beattie et al., 1994; Brault et al., 1997; Edmondston et al., 2000; Fennell

et al., 1996). No data exists for coronal plane positioning.

However, there were several isolated cases where deformation direction was opposite in

normal discs and this has also been reported in the literature. A possible mechanism for

this finding may be that tensile forces in the inner anulus unilaterally exceed

compressive forces on the opposite side. The net force will then be directed towards the

compressive load rather than away. However, such an hypothesis has not been tested. In

general NP deformation is highly predictable in the sagittal and coronal planes.

Far less predictability of NP deformation direction was seen subsequent to axial rotation

in young normal subjects. The effect on predictability of NP deformation with the

addition of the variables flexion or extension co-positioning was examined in a small

group, and reported in the pilot study (Appendix 4). The unpredictability of NP

deformation was was shown in a larger group in the normative cohort MRI study

(chapter 5) where it was reported that 56% of NPs deformed contralateral to the

direction of rotation and 44% ipsilaterally. However this latter study demonstrated that

75% of NPs deformed contralaterally to the direction of conjunct lateral flexion, thereby

prompting the lateral flexion cohort MRI study (chapter 6). Additionally it was seen that

Page 155: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 10: Discussion

Page X-5

95% deformed inversely in response to sagittal plane positioning. The general trends for

NP deformation direction relative to positioning are depicted in Figure 10.2.

Figure 10.2: Direction of NP deformation following coronal (lateral flexion) axial (rotation) and sagittal (flexion) positioning.

A reasonable conclusion from these results is that the predictability of direction of

deformation relates to available intersegmental range of motion in any given direction.

Axial rotation (with the smallest range of motion) is least predictable (approximately

50%) while coronal (95%) and sagittal (95%) planes clearly show stronger

predictability associated with greater ranges of motion.

10.3.3.2 Magnitude of NP deformation

The magnitude of NP deformation was reported as a mean percentage.

Using the peak pixel tracking method the pilot study (Appendix 4) showed a 19%

lateral deformation of the NP when subjects were positioned in rotation plus extension

and 9% when positioned in rotation plus flexion. These figures are greater than those of

Page 156: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 10: Discussion

Page X-6

the normative cohort MRI study (chapter 5) which reported a mean of 5.5%. Both these

studies positioned subjects in flexion and extension therefore differences cannot be

ascribed to positioning. The variation in the pilot study (Appendix 4) differs from the

literature which reports greater segmental rotation in flexion and less in extension

(Burnett et al., 2008; Pearcy et al., 1984; Pearcy & Tibrewal, 1984; Pearcy, 1993;

Pearcy & Hindle, 1991).

Deformation magnitude in the lateral flexion cohort study (chapter 6) averaged 16.4%.

This was greater at the apex of the curve and less at the superior and inferior regional

limits. Greater subject numbers, plus the inclusion of all lumbar segments in this study

enabled a more thorough analysis. The magnitude was generally greater than that seen

in the rotation studies, though less than that seen in the pilot study (Appendix 4) where

sagittal plane data was assessed.

It would be reasonable to conclude from these results that the predictability of NP

deformation direction is relative to the magnitude of available intersegmental range in

any cardinal plane. However, the magnitude of NP deformation was found not to be

proportional to the magnitude of intersegmental range.

10.4 Theme two – what is the effect of age and deformity?

The second series of studies including the older cohort MRI study (chapter 7), the

scoliosis cohort MRI study (chapter 8) and the longitudinal case study (chapter 9)

applies the previously developed method to cohorts with degnerative IVD changes plus

those with a primary spinal deformity. While it can be argued that degenerative change

is consequential to normal ageing rather than a pathology, it is included here to

complement observations drawn from the young normal population.

10.4.1 Ageing discs

The older cohort MRI study (chapter 7) reports a study of subjects aged between 40 and

57, years with variable degenerative change in some or all lumbar discs. Few studies

have investigated changes to NP signal in sagittal plane positions and none have

investigated rotation effects. Reference was made to differences in aged discs in only

one related study (Edmondston et al., 2000), concluding that directional bias was less

predictable in older discs. This is the first such study to report NP deformation specific

to rotation in graded degenerated discs.

Page 157: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 10: Discussion

Page X-7

NP deformation is fundamentally governed by hydrodynamic principles. Degenerative

change within the IVD primarily results in loss of fluid, reduction in disc height and

subsequent modification of load bearing (see chapter 2, section 2.2). Other mechanical

changes result, including increased intersegmental range of rotation as reported in

chapter 4. The interrelationship of these changes raises the question as to the effect of

IVD degeneration on NP deformation resulting from axial rotation and how this might

differ from the normal.

Using the same image analysis protocol described in the normative and lateral flexion

cohort MRI studies (chapters 5 and 6), the older cohort MRI study (chapter 7) showed a

mean coronal NP deformation of 2.3%, less than half the normative data reported in

chapter 5. The magnitude of change in the NP deformation was therefore most evident

in the younger cohorts where the NP signal could be clearly seen offset from the

compression load axis. In contrast, the older cohort showed NPs with lower signal and

for whom the NP deformation was both less evident and smaller in magnitude.

Consequently, the results for the older cohorts challenge the utility of the current

method given that the measurement error is slightly greater than the mean change

recorded for those discs with correspondingly more pronounced degenerative changes.

A trend towards deformation being greater at L1-2 may be explained by fewer cases

with degenerative change in the upper lumbar levels.

In the older cohort, directional bias was similar to the normative (younger) cohort, with

approximately half of the NPs deforming towards the left (47.3%) and half right

(52.7%). When this was compared with the direction of segmental lateral flexion it was

seen that 61.8% deformed to the contralateral side. This is less than the 75% reported in

the normative cohort MRI study (chapter 5). Gender bias in direction is noted and

unexplained, possibly reflecting the small number of cases.

On the basis of these results it would be reasonable to dispute the propositions in the

literature that NP deformation direction is less predictable in discs with degenerative

change (Edmondston et al., 2000; Modic & Ross, 2007). Caution should be exercised as

these two studies employ an alternative method, using T2 weighted MR images and a

pixel intensity method applied to sagittal images, with only a single line transect across

the mid disc region.

Page 158: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 10: Discussion

Page X-8

Comparison between results in the normative and older cohort MRI studies (chapters 5

and 7) also warrants circumspection, in recognition of the method variable of sagittal

plane positioning which was used only in the normative cohort study (chapter 5).

While it is stated that water loss in the IVD reduces hydrostatic properties evidence is

not forthcoming to support this (Modic & Ross, 2007). The study in chapter 7 disputes

this claim as predictability is unaffected; only the magnitude of the hydrostatic effect is

reduced.

As the IVD loses water content the T2 weighted MRI signal reduces and reveals a

patchy hydration pattern (Figure 10.3). Areas of retained hydration will likely continue

to behave hydrostatically but the inconsistent distribution would reduce the overall

effect. Claims of reduced predictability may be an effect of single line samples being

less representative of the whole IVD.

Degenerative change is often accompanied by formation of clefts between concentric

anular rings. This may allow extrusion of NP material into these clefts, further

redistributing NP and rendering hydration difficult to ascertain from single line pixel

samples in the sagittal plane. Multiple line samples, as used in chapter 7, particularly

from axial images, have a greater likelihood of capturing signal from NP infiltration of

anular clefts and therefore inclusion in any quantification of NP deformation.

24 year old male 48 year old male

Figure 10.3: Three dimensional surface plot profile of pixel intensity signal from T2

weighted axial MRI showing normal hydration patterns (A) with clearly increased signal from NP and (B) patchy hydration and markedly reduced signal intensity from

the NP of a degenerate disc. As the NP loses hydrostatic pressure its load attenuation ability is compromised while

the AF takes more load (Figure 10.4). This reversal of proportional load bearing may

also contribute to reduced NP deformation as pressure from the AF and associated

A B

Page 159: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 10: Discussion

Page X-9

inward buckling of the inner anular fibres (Meakin et al., 2001) (Figure 10.5) may

further constrain the NP generally.

Figure 10.4: Loss of NP fluid content in degenerative disc disease (DDD) leading to increased loading of AF may contribute to reduced NP deformation magnitude.

Figure 10.5: Inward buckling of inner anular fibres (arrow) may constrain NP

deformation. (Adapted from Adams, 2002)

Nucleus pulposus deformation in response to axial rotation has therefore been shown to

be less predictable than positioning in the sagittal and coronal planes but similarly

predictable between younger and older subjects.

10.4.2 Scoliosis

Scoliosis is the only multiplanar structural deformity that typically includes changes in

both coronal and axial planes. Since these are the two primary planes considered as

variables in this thesis, scoliosis provides an ideal clinical model from which to examine

the effect of a long standing multiplanar structural deviation on IVD deformation.

Page 160: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 10: Discussion

Page X-10

The mechanics of scoliosis and the presenting deformity are described in the scoliosis

cohort MRI study (chapter 8).

10.4.2.1 Range of lateral flexion in scoliosis

Chapter 8 reports data obtained from the intervertebral level at the apex of secondary

lumbar scoliotic curves. Most often the peak of the lumbar curve occurred at L2-3

(50%) followed by T12-L1 (28%) and the mean intersegmental lateral flexion angle was

7.5°. In the normal subjects reported in the lateral flexion cohort MRI study (chapter 6)

the most common lumbar lateral flexion apex was L3-4 and the range of intersegmental

lateral flexion at each segment averaged 6.1°.

This relatively small difference in mean ranges may result from segmental level

variations or the effect of averaging over all lumbar segments. Additionally, the subjects

in the lateral flexion cohort MRI study (chapter 6) were placed and constrained into end

range lateral flexion while those in the scoliosis cohort MRI study (chapter 8) were

positioned without imposed postural constraint and therefore not necessarily at the end

range of segmental lateral flexion.

While much data exists on the degree of curvature of the scoliotic spine it describes

predominantly the primary thoracic curve as measured by the method described by

Cobb, rather than measurements of specific intersegmental angles. Few comparative

data exist for segmental ranges in secondary lumbar scoliotic curves.

10.4.2.2 Range of rotation in scoliosis

The direction of segmental rotation in the scoliosis cohort MRI study (chapter 8) was

ipsilateral to the coronal deformity in all cases. This is a function of the complex and

poorly understood etiology of scoliosis (Kouwenhoven & Castelein, 2008).

Mean segmental rotation between the vertebral bodies adjacent to the apical IVD was

4.6°. In contrast, the lateral flexion cohort MRI study (chapter 6) reports much smaller

ranges, however rotation was only coincident as primary positioning was into lateral

flexion. Comparison is therefore limited. Additionally, rotation in scoliosis occurs not

only at the IVD level but within the bodies of the vertebrae (Birchall et al., 2005) so

cannot accurately be termed intersegmental. Few comparative data exist for segmental

rotation angles in secondary lumbar curves of scoliotic spines.

Page 161: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 10: Discussion

Page X-11

10.4.2.3 NP deformation

Mean coronal plane NP deformation in scoliotic spines was 12.9% while that of normal

subjects was 11.3%. This small difference may be a function of data being derived from

apical segments rather than averaged from all lumbar levels. In each scoliotic case the

deformation direction was towards the convexity. In contrast, in 4/105 of the discs in

normal laterally flexed subjects (chapter 6) the deformation was away from the

convexity.

There was no association between NP deformation magnitude and degree of segmental

lateral flexion in the scoliotic curves, however a moderate association existed in the non

scoliotic spines reported in the lateral flexion cohort MRI study (chapter 6). This

association needs to be tested with greater subject numbers for a more thorough

comparison. It is hypothesised that at best a poor association occurs at extremes of

range, where the creep effect allows further increase in lateral flexion range but the

tensile force in intact inner anular fibres prevents further NP deformation. This could be

tested by gathering data on NP deformation at selected sub maximal ranges of lateral

flexion.

Scoliosis is a rare topic area in which IVD hydration has been discussed in the

literature. A method of three dimensional mathematical modelling of the NP in scoliosis

has been developed and reported (Périé et al., 2001). This was later used to characterise

NP migration in response to mechanical effects but only in coronal and sagittal planes

(Périé et al., 2003). Migration to the convexity was reported in all cases and was

consistent with chapter 8 conclusions.

A similar method was validated and used by Violas pre and post operatively in scoliosis

to examine the effect on non stabilised lumbar discs (Violas et al., 2007a, b; Violas et

al., 2005). Quantification of both NP and whole disc volume was reported, without

consideration of variations of hydration pattern within the IVD or specific reference to

axial plane movement changes or influence on such patterns.

The scoliosis cohort MRI study (chapter 8) takes this concept further, not only

supplying directional data but also mapping of hydration patterns within the NP.

Additionally, axial plane influence on hydration patterns is considered where other

investigators have not. The chapter 8 study does not attempt to quantify total disc

hydration.

Page 162: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 10: Discussion

Page X-12

In general scoliotic motion segments analysed in chapter 8 showed a more consistent

NP deformation directional bias than those of non scoliotic spines in chapters 4-7. As

rotation and lateral flexion components of the deformity always occur in tandem it is

not possible to separate the effect of coronal and axial plane positioning. The preceding

studies suggested that lateral flexion direction more strongly predicts deformation

direction. However, clarification of this question may not be assisted by examining

scoliotic spines, given the triplanar nature of that pathology.

10.4.3 IVD herniation

IVD herniation is a common injury frequently caused by rotation strains (Scannell &

McGill, 2009) and the most frequently occurring primary pathology involving extrusion

of NP material (Moore et al., 1996). The effect is to disrupt the internal homeostasis of

the disc, thereby potentially altering its mechanical properties and ability to attenuate

load. Figure 10.4 represents the mechanism by which altered load bearing results from

loss of NP hydration over time. Herniated NP also effectively reduces the hydration

volume as some NP material escapes the disc interior. This may contribute to

accelerated onset of degeneration (Farfan et al., 1970). Even minor disruption of the AF

during discography has been shown to contribute to early degenerative change

(Carragee et al., 2004).

The longitudinal case study (chapter 9) considers this primary rotational and NP-related

pathology and reports a unique longitudinal case study of variables other than NP

deformation. These include tracking cross sectional area of lumbar multifidus and the

thecal sac, in addition to fat infiltration of multifidus over a 12 year period. The findings

are compared with the relevant literature. While these parameters have been previously

reported for both the cervical (Elliott et al., 2008) and lumbar (Hides et al., 2008)

regions, they have not been tested over such an extended timeframe subsequent to

lumbar rotational injury and NP changes due to loss of intradiscal structural integrity.

The protracted duration of this longitudinal study permits reporting of late changes in

muscle cross sectional area and fat infiltration, and the prospect for restoration with

exercise after long established injury.

Page 163: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 10: Discussion

Page X-13

10.4.3.1 NP deformation

The deformation of the NP following AF disruption is macroscopically evident. In the

reported longitudinal case study (chapter 9), the direction was central into the spinal

canal where it tracked superiorly along the theca. This was measured and changes

followed in thecal sac A-P dimension. Clearly NP deformation was markedly greater

than the previous studies in Appendix 4 and chapter 5 which included flexion

positioning as these subjects retained intact anuli.

Directional bias depends upon the location of AF disruption. Predisposition to certain

locations for AF disruption may be pre-existent and associated with underlying anular

tears which may lead to the formation of clefts (Osti et al., 1990). As flexion has been

shown to deform the NP posteriorly in the majority of cases the occurrence of NP

herniation in the posterior half of the disc is unsurprising. The rotational component of

the injuring mechanism would in theory have a different effect. It has been shown that

increasing intersegmental rotation causes the axis of motion to migrate towards the

compression facet (Wachowski et al., 2009). This would result in the greatest force

being directed at the point most distant from the axis – in this case the anterolateral

anulus. If rotation was the dominant causative factor then herniations would occur in

that region. The predilection of herniations for the posterior anulus suggests that flexion

is more dominant in causation. The anatomical variation in AF depth between anterior

and posterior is also a contributing factor.

Further direct comparison with previous studies in chapters 5-8 beyond the sagittal

plane is invalid as positioning for MRI was neutral with no coronal or axial component.

10.4.3.2 Fat infiltration and cross sectional area

Fat infiltration and cross sectional area (CSA) of multifidus are reported in the

longitudinal case study (chapter 9) and vary somewhat from previous reports in the

literature. Reduction in cross sectional area is reported to be specific to the side of

symptoms and the intervertebral level involved (Hides et al., 1994). Chapter 9 also

reports a reduction in cross sectional area but it is neither isolated to the intervertebral

level of herniation nor the side of symptoms. Multifidus contains both long and short

fascicles, the latter crossing several segments between bony attachments (Rosatelli et

al., 2008). A cross sectional sample at a given level will therefore capture both, however

not all necessarily have direct connection to that level. It could therefore be expected

Page 164: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 10: Discussion

Page X-14

that atrophy would be evident at other levels within the region (as reported in the

longitudinal case study in chapter 9) which also shows changes bilaterally.

The literature reports a reduction in Multifidus CSA post injury but proposes that this

does not reverse spontaneously unless very specific exercises are undertaken (Hides et

al., 1996). Chapter 9 results do not support this theory as an increase in CSA was seen

12 years post injury without intervention beyond an increase in normal activity level

over time.

Fat infiltration followed a similar trend, with an initial increase post injury and

reduction at 12 years raising the possibility of association with CSA.

10.5 Limitations

Identification of study limitations are important to avoid over interpretation and

inappropriate extrapolation. The limitations relevant generally across the study series

will be elaborated.

10.5.1 Samples

Convenience samples were used in each of the cohort studies to generate and test

hypotheses. It is not intended that the sample sizes were adequate for full statistical

analysis, rather to describe and report preliminary trends. Recommendations for future

studies (chapter 11) addresses several areas where larger samples of more homogeneous

cohorts (age, disease, deformity) could be assessed.

10.5.2 Magnetic Resonance Imaging

All MRI studies were undertaken in a conventional closed magnet. This limited subject

selection to those of a body size and shape amenable to positioning within the confines

of the magnet bore. Subject selection was also limited by general contraindications to

MRI as defined in Appendix 3. The conventional nature of the magnet requires non-

weighbearing positioning of subjects limiting functional relevance of results.

Evolution of novel method changes over a 7 year study period, incorporating a change

in MRI unit from a 1 Tesla to a 1.5 Tesla model, meant no retrospective pooling and

comparisons were possible. However, general trends were noted across cohort studies.

During the course of the various studies four different MRI technologists provided

support during scheduled weekend research blocks. Subtle differences in approaches to

acquisition of the different sequences, despite written protocols, may have meant the

Page 165: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 10: Discussion

Page X-15

image data were not entirely consistent. This is especially so for determining coronal

slice position used to define lateral flexion angles.

10.5.3 Data comparison

Data derived from each cohort reflected mixed gender and age samples which

contributed to the variability within these data sets.

10.6 Clinical implications

The results from these studies reveal NP deformation direction to be highly predictable

in the sagittal and coronal plane but not in the axial plane. Magnitude of NP

deformation and range of segmental movement are not strongly associated.

There are several practical implications of this new knowledge.

A commonly used intervention for management of low back pain is predicated on the

presumption that discogenic pain results from NP deformation against a damaged and

pain sensitive anulus (McKenzie & May, 2003). Passive and active movements and

postures in sagittal, coronal and axial planes are employed on this basis to impart a

predictable mechanical effect on the NP position. MRI studies of NP deformation will

provide the basis for a better understanding of these interventions and their mechanical

effects.

Postural scoliosis in acute low back pain is common and associated with lumbar disc

injury and sciatica (Akhaddar et al., 2011). Advanced knowledge of IVD and NP

mechanics will elaborate the potential mutability of the NP to corrective mechanical

forces in internal disc disruption. Limited case based evidence exists for this concept

and it association with symptom reduction (Appendix 5).

Torsional anular injury may result in frank NP herniation. Better understanding of the

mechanical effect of primary plane movement and position through such MRI based

studies may help inform conservative management protocols.

Better understanding of lumbar NP behaviour relative to positioning will potentially

assist in further development of artificial discs.

Page 166: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 10: Discussion

Page X-16

Perianular ossification related to loss of rotation control has been reported (Fraser et al.,

2004). This may be avoided with expanded knowledge of the mechanical effects of

rotation on the NP.

NP replacement is also becoming more frequent and its refinement will benefit from

such knowledge (Coric & Mummaneni, 2008; Puentedura et al., 2010). Replication of

the complex biomechanical properties of the motion segment using such biodevices is

challenging and requires detailed knowledge of normal mechanics (Costi et al., 2011).

Knowledge of NP deformation patterns may also inform the study of ergonomics from a

better understanding of biomechanics to minimise posterior anular wall strain relative to

lumbar position.

Page 167: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 10: Discussion

Page X-17

References

Adams M, Bogduk N, Burton K, Dolan P. The Biomechanics of Back Pain. London,: Churchill Livingstone, 2002.

Akhaddar A, Belfquih H, Oukabli M, Boucetta M. Posterior ring apophysis separation combined with lumbar disc herniation in adults: a 10-year experience in the

surgical management of 87 cases. J Neurosurg Spine 2011; 14(4): 475-83. Alexander LA, Hancock E, Agouris I, Smith FW, MacSween A. The response of the

nucleus pulposus of the lumbar intervertebral discs to functionally loaded

positions. Spine 2007; 32(14): 1508-12. Beattie PF, Brooks W, Rothstein J. Effect of lordosis on the position of the nucleus

pulposus in supine subjects. Spine 1994; 19: 2096-102. Birchall D, Hughes D, Gregson B, Williamson B. Demonstration of vertebral and disc

mechanical torsion in adolescent idiopathic scoliosis using three-dimensional

MR imaging. Eur Spine J 2005; 14(2): 123-9. Brault J, Driscoll D, Laakso L, Kappler R, Allin E, Glonek T. Quantification of lumbar

intradiscal deformation during flexion and extension by mathematical analysis of magnetic resonance imaging pixel intensity profiles. Spine 1997; 22: 2066-72.

Burnett A, O'Sullivan P, Ankarberg L, Gooding M, Nelis R, Offermann F, Persson J. Lower lumbar spine axial rotation is reduced in end-range sagittal postures when

compared to a neutral spine posture. Man Ther 2008; 13(4): 300-6. Carragee EJ, Barcohana B, Alamin T, van den Haak E. Prospective controlled study of

the development of lower back pain in previously asymptomatic subjects

undergoing experimental discography. Spine 2004; 29(10): 1112-7. Coric D, Mummaneni PV. Nucleus replacement technologies. J Neurosurg Spine 2008;

8(2): 115-20. Costi JJ, Freeman BJ, Elliott DM. Intervertebral disc properties: challenges for

biodevices. Expert Rev Med Devices 2011; 8(3): 357-76.

Edmondston S, Song S, Bricknell R, Davies P, Fersum K, Humphries P, Wickendon D, Singer K. MRI evaluation of lumbar spine flexion and extension in

asymptomatic individuals. Manual Therapy 2000; 5: 158-64. Elliott J, Sterling M, Noteboom JT, Darnell R, Galloway G, Jull G. Fatty infiltrate in the

cervical extensor muscles is not a feature of chronic, insidious-onset neck pain.

Clin Radiol 2008; 63(6): 681-7. Farfan HF, Cossette JW, Robertson GH, Wells RV, Kraus H. The effects of torsion on

the lumbar intervertebral joints: the role of torsion in the production of disc degeneration. J Bone Joint Surg Am 1970; 52(3): 468-97.

Fennell A, Jones A, Hukins D. Migration of the nucleus pulposus within the

intervertebral disc during flexion and extension of the spine. Spine 1996; 21: 2753- 7.

Fraser R, Ross E, Lowery G, Freeman B, Dolan M. Lumbar disc replacement Acroflex design and results. The Spine Journal 2004; 4: 245s-51s.

Haughton V, Rogers B, Meyerand M, Resnick D. Measuring the axial rotation of

lumbar vertebrae in vivo with MR imaging. American Journal of Neuroradiology 2002; 23: 1110-6.

Hides JA, Gilmorea C, Stanton W, Bohlscheida E. Multifidus size and symmetry among chronic LBP and healthy asymptomatic subjects. Manual Therapy 2008; 13: 43-9.

Hides JA, Richardson CA, Jull GA. Multifidus muscle recovery is not automatic after resolution of acute, first-episode low back pain. Spine 1996; 21(23): 2763-9.

Page 168: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 10: Discussion

Page X-18

Hides JA, Stokes MJ, Saide M, Jull GA, Cooper DH. Evidence of lumbar multifidus

muscle wasting ipsilateral to symptoms in patients with acute/subacute low back pain. Spine 1994; 19(2): 165-72.

Johansen JG, Nork M, Grand F. Torsional instability of the lumbar spine. Rivista di Neuroradiologia 1999; 12: 193-5.

Keyes D, Compere E. The Normal and pathological physiology of the nucleus pulposus

of the intervertebral disc: an anatomical, clinical, and experimental study. The Journal of Bone and Joint Surgery 1932; 14: 897-938.

Kouwenhoven JW, Castelein RM. The pathogenesis of adolescent idiopathic scoliosis: review of the literature. Spine 2008; 33(26): 2898-908.

Kramer J. Intervertebral disc diseases. Causes, diagnosis, treatment and prophylaxis. .

Chicago: Year Book Medical Publishers, Inc, 1981. McKenzie R, May S. Mechanical Diagnosis and Therapy, 2 ed. Waikanae: Spinal

Publications New Zealand Ltd, 2003. Meakin JR, Redpath TW, Hukins DW. The effect of partial removal of the nucleus

pulposus from the intervertebral disc on the response of the human annulus

fibrosus to compression. Clin Biomech (Bristol, Avon) 2001; 16(2): 121-8. Modic MT, Ross JS. Lumbar degenerative disk disease. Radiology 2007; 245(1): 43-61.

Moore RJ, Vernon-Roberts B, Fraser RD, Osti OL, Schembri M. The origin and fate of herniated lumbar intervertebral disc tissue. Spine 1996; 21(18): 2149-55.

Osti OL, Vernon-Roberts B, Fraser RD. 1990 Volvo Award in experimental studies.

Anulus tears and intervertebral disc degeneration. An experimental study using an animal model. Spine 1990; 15(8): 762-7.

Pearcy M, Portek I, Shepherd J. Three-dimensional x-ray analysis of normal movement in the lumbar spine. Spine 1984; 9(3): 294-7.

Pearcy M, Tibrewal S. Axial rotation and lateral bending in the normal lumbar spine

measured by three-dimensional radiography. Spine 1984; 9: 582-87. Pearcy MJ. Twisting mobility of the human back in flexed postures. Spine 1993; 18(1):

114-9. Pearcy MJ, Hindle RJ. Axial rotation of lumbar intervertebral joints in forward flexion.

Proc Inst Mech Eng [H] 1991; 205(4): 205-9.

Périé D, Curnier D, de Gauzy JS. Correlation between nucleus zone migration within scoliotic intervertebral discs and mechanical properties distribution within

scoliotic vertebrae. Magn Reson Imaging 2003; 21(9): 949-53. Périé D, Sales De Gauzy J, Curnier D, Hobatho M. Intervertebral disc modeling using a

MRI method : migration of the nucleus zone within scoliotic intervertebral discs.

Magnetic Resonance Imaging 2001; 19(9): 1245-8. Puentedura EJ, Brooksby CL, Wallmann HW, Landers MR. Rehabilitation following

lumbosacral percutaneous nucleoplasty: a case report. J Orthop Sports Phys Ther 2010; 40(4): 214-24.

Rosatelli AL, Ravichandiran K, Agur AM. Three-dimensional study of the

musculotendinous architecture of lumbar multifidus and its functional implications. Clin Anat 2008; 21(6): 539-46.

Scannell JP, McGill SM. Disc prolapse: evidence of reversal with repeated extension. Spine 2009; 34(4): 344-50.

Singer K, Svansson G, Day R, Breidahl W, Horrex A. The utility of diagnosing lumbar

rotational instability from twist CT scans. Journal of Musculoskeletal Research 2001; 5: 45-51.

Violas P, Estivalezes E, Briot J, Sales de Gauzy J, Swider P. Objective quantification of intervertebral disc volume properties using MRI in idiopathic scoliosis surgery. Magn Reson Imaging 2007a; 25(3): 386-91.

Page 169: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 10: Discussion

Page X-19

Violas P, Estivalezes E, Briot J, Sales de Gauzy J, Swider P. Quantification of

intervertebral disc volume properties below spine fusion, using magnetic resonance imaging, in adolescent idiopathic scoliosis surgery. Spine 2007b;

32(15): E405-12. Violas P, Estivalezes E, Pedrono P, Sales de Gauzy J, Sevely A, Swider P. A method to

investigate intervertebral disc morphology from MRI in early idiopathic

scoliosis: a preliminary evaluation in a group of 14 patients. Magnetic Resonance Imaging 2005; 23: 475-9.

Wachowski MM, Mansour M, Lee C, Ackenhausen A, Spiering S, Fanghanel J, Dumont C, Kubein-Meesenburg D, Nagerl H. How do spinal segments move? J Biomech 2009; 42(14): 2286-93.

White A, Panjabi M. Clinical Biomechanics of the Spine, 2nd ed. Philadelphia: Lippincott, 1990;

Page 170: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

CHAPTER 11

Page XI-1

Conclusions and recommendations

The primary purpose of this thesis investigation was to quantify the in vivo effect of

rotation postures on lumbar NP deformation and to report the predictability of the

direction of that deformation. Additionally, the effects of coincident coronal plane

positions, age related changes and spinal deformity (scoliosis) were examined to

determine the relative influences of such factors on the internal mechanism of the IVD.

The principal hypothesis was that the NP would deform in all cases and conditions in a

predictable direction and with a magnitude proportional to the resultant segmental

angulation.

Secondary hypotheses, tested in the individual investigations that form the complete

series, are addressed below.

The primary method for measuring NP deformation magnitude was shown to be

reliable.

11.1 The ex vivo CT study (chapter 4)

The objective of this study was to examine the influence of lumbar zygapophysial joint

anatomy and intervertebral disc pathology on axial torsion response in ex-vivo

ligamentous lumbar spine preparations using 3D motion tracking and computed

tomography (CT). This study concluded that:

1. Axial rotation and joint separation was greatest for the lower lumbar segments

which corresponded with larger coronal joint angles.

2. Semi-flexion generally resulted in increased segmental rotation compared with

neutral and extension positions, except in the presence of marked segmental

degeneration.

3. Separation of the zygapophysial joint is a normal response during axial rotation

movements. However, anatomical configuration of the paired zygapophysial

joints, and the stage of degenerative disc disease impacts on segmental mobility.

This study generated the hypotheses which informed the following studies.

Page 171: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 11: Conclusions and recommendations

Page XI-2

11.2 The pilot study (appendix 1)

The aim of this study was to assess a novel method using MRI to track NP deformation

following positioning into flexion and extension, and the combined positions of flexion

plus left rotation and extension plus left rotation in the lumbar spine, at L1-2 and L4-5.

This study concluded that:

1. The method was reliable.

2. That a predictable pattern of anterior NP deformation was evident following a

change in sagittal plane position from one of flexion to extension in the target

intervertebral discs.

3. There was a trend to NP deformation to the right with the addition of left

rotation positioning.

11.3 The normative cohort MRI study (chapter 5)

This study was designed to test the hypothesis that NP deformation subsequent to

sagittal, axial and conjunct coronal plane positioning would demonstrate predictable

directionality. Results showed that NP deformation direction was highly predictable

following sagittal plane position change as 19/20 cases deformed towards the convexity.

Axial plane positioning into left rotation showed 44% of NPs deformed to the left and

56% deformed to the right. In 75% of cases the NP deformed to the opposite side to

coincident intersegmental lateral flexion.

The following conclusions were therefore drawn:

1. The hypothesis was accepted with respect to sagittal plane positions as results

demonstrated that the direction of NP deformation after lumbar sagittal plane

positional change was predictable.

2. Deformation of the NP following adoption of rotated positions in flexion and

extension was reduced in magnitude and less predictable with respect to

direction.

3. That the direction of coincident intersegmental lateral flexion was a stronger

predictor of NP deformation direction than axial rotation direction.

11.4 The lateral flexion cohort MRI study (chapter 6)

This study sought to assess the effect of coronal plane positioning alone on NP

deformation. This tested the hypothesis that the NP would deform predictably towards

Page 172: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 11: Conclusions and recommendations

Page XI-3

the convexity and with a magnitude proportional to the range of segmental lateral

flexion. Reported results were:

1. That the NP displaced away from the direction of lateral flexion in 95/105 discs

(P<0.001).

2. That the extent of NP displacement was associated strongly with lateral flexion

at L2-3 (P<0.01).

3. The greatest range of lateral flexion occurred at L2-3, L3-4 and L4-5. Small

intersegmental ranges of axial rotation occurred at all levels but were not

associated with NP displacement.

From these results the following conclusions were drawn:

1. Direction of NP deformation was highly predictable in laterally flexed healthy

lumbar spines.

2. The magnitude of displacement was not commensurate with the degree of

intersegmental lateral flexion or rotation.

Consequently the hypothesis that magnitude would be proportional to the degree of

lateral flexion was rejected and the hypothesis that NP deformation would be towards

the convexity was accepted.

11.5 The older cohort MRI study (chapter 7)

The purpose of this study was to test the influence of age related changes on NP

deformation and therefore to test the hypotheses that greater segment lateral flexion and

rotation would induce the largest NP deformation from the neutral position; that more

severe disc degeneration would reduce the extent of any NP deformation and that the

NP would deform contralaterally to the direction of segmental lateral flexion.

Mean NP deformation was 2.1% of disc width. At L3-4 there was a modest association

between lateral flexion and NP deformation (r=0.38, p<0.034). In the left rotation

position 47.3% of all discs deformed to the left and 52.7% to the right; 61.8% deformed

contralateral to the direction of intersegmental lateral flexion. The following

conclusions are therefore drawn:

1. NP deformation magnitude was independent of level, grade of degeneration or

segmental lateral flexion or rotation angle.

2. The direction of NP deformation was unpredictable in rotation and poorly

predictable with respect to lateral flexion direction.

Page 173: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 11: Conclusions and recommendations

Page XI-4

3. The degree of degeneration did not appear to be associated with predicting the

deformation direction.

Consequently the hypotheses concerning rotation and the influence of stages of

degeneration were rejected. The hypothesis that NP deformation would occur

contralateral to the direction of segmental lateral flexion was accepted.

11.6 The scoliosis cohort MRI study (chapter 8)

This retrospective observational cohort study was undertaken to test the hypothesis that

in lumbar compensatory scoliotic curves, NP deformation magnitude at the apex of the

curve would be associated with the extent of intersegmental lateral flexion range.

Lumbar Cobb angles ranged from 12.4° to 54.6°, with a mean of 34.9°. Intersegmental

rotation at the apex ranged from 0.8° to 8.0°, with a mean of 4.6°. Segmental lateral

flexion ranged from 4.2° to 13.7°, with a mean of 7.5°. The apical NP showed an offset

away from the midline which was not associated with the extent of the Cobb angle

(r=0.12).

Adolescent lumbar compensatory scoliosis results in exaggeration of the three cardinal

planes which coupled with disc wedging contribute to an offset deformation of the NP

away from the compressive axis. While in general, the greater the disc wedging and

lumbar Cobb angles the further the displacement of the NP, there was no association

between magnitude of NP deformation and extent of Cobb angle. The hypothesis was

therefore rejected.

11.7 The longitudinal case study (chapter 9)

This 12 year retrospective longitudinal single case study followed the natural history of

a rotation injury to the IVD resulting in a large central L4-5 disc herniation. It assessed

variables including herniation size and the effect on paravertebral muscle cross sectional

area and degree of fat infiltration. It tested the hypothesis that changes in paravertabral

muscle size and composition occur with normal activity after 12 years. Changes in cross

sectional area and fat infiltration demonstrated restoration over the course of the study.

The hypothesis was therefore accepted.

Page 174: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 11: Conclusions and recommendations

Page XI-5

11.8 Recommendations for future studies

The series of studies presented in this thesis were designed to test the hypotheses as

described. Investigation of these raised further questions which could be tested in the

following proposed studies:

11.8.1 Larger cohort, three dimensional weightbearing study

A future study employing the refined method described in chapter 7 applied to a larger

cohort of subjects would be of interest. This would allow age and gender matched

analysis of results to examine for statistically significant differences. This could also

include the addition of subject positioning into both left and right rotation to test for

intra subject laterality difference in NP deformation. Ideally image acquisition would

occur within an open MRI permitting physiological loading. This would require rapid

image sequencing but would also allow a greater variety of positions to be examined,

with consideration of the functional implications of derived data.

Three dimensional image analysis may better quantify fluid shift within the confines of

the anulus and more accurately characterize directional predictability.

11.8.2 Ex vivo islolated segmental rotation study

The aim of this study would be to examine the effect of isolated intersegmental rotation

on NP deformation direction and magnitude. In vivo coupling of motion in axial and

coronal planes makes difficult the analysis of the effect of positional change in each

separately.

A torsion rig similar to that used in the ex vivo study described in chapter 4 would be

constructed with non ferrous material. Into this would be fixed a cadaveric lumbar spine

section comprising cojacent vertebral bodies and the intervening intervertebral disc with

all muscular and ligamentous attachments removed. Through an external pulley system

attached to the vertebral bodies, predetermined incremental loads would be applied to

induce isolated positional change in the cardinal planes.

The rig would be placed in an MRI scanner and a protocol employed to acquire axial,

coronal and sagittal T1 and T2 weighted images.

Image analysis in three dimensions would characterise and quantify direction of NP

deformation relative to each position and load. From this data the contribution of each

component of composite in vivo motion may be better understood.

Page 175: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 11: Conclusions and recommendations

Page XI-6

Preferably human material would be tested but in its absence a suitable animal surrogate

such as sheep lumbar segments could substitute (Wilke et al., 1997). Morphological and

therefore biomechanical differences between the human spine designed for bipedal

locomotion and that of a quadruped would require consideration.

11.8.3 Clinical studies

11.8.3.1 Diagnosis of discogenic pain

The primary tissue source of pain in localized, non specific low back pain cannot be

accurately determined clinically especially with reference to discogenic pain (Adams et

al., 2002). Centralisation and peripheralisation of pain correlates with proven discogenic

pain (Donelson et al., 1997) but is not considered to be diagnostic (Bogduk & Lord,

1997).

While it is accepted that low back pain is a multi structure problem, an ability to

clinically differentiate the relative contribution of disc and zygapophysial joints would

improve treatment specificity and accurately direct further investigation.

The studies described in this thesis identify greater predictability of NP deformation in

sagittal and coronal plane positioning. Most functional activities require concurrent

motion through several planes. Clinical movement examination should therefore extend

beyond the cardinal planes to combinations (Barrett et al., 1999; Edwards, 1992).

In light of reported results, clinical examination of combinations founded on sagittal and

coronal planes may ensure better predictability and understanding of the NP response.

Patterns of symptom response may elucidate potential tissue sources of pain. The

potential for combined movement to identify structural or tissue source has been

postulated (Singer et al., 2004).

Subjects with non specific low back pain would be examined with combined sagittal

and coronal plane movements using three dimensional motion analysis (Figure 11.1).

Pain and movement maps will be derived from this assessment (Barrett et al., 1999).

Results will be correlated with reproduction of concordant pain on discography or

amelioration of symptoms on zygapophysial joint block to identify primary pain source.

Page 176: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 11: Conclusions and recommendations

Page XI-7

Such a study as described may contribute new knowledge to clinical diagnosis and

management of low back pain.

Figure 11.1: Three dimensional motion analysis has been shown to be a reliable

method for mapping movement patterns in the Lumbar spine. (From Barrett et al, Man

Ther 1999; 4(2): 94-9).

11.8.3.2 Scoliosis

The study described in chapter 8 examined only the apical disc of the secondary lumbar

curve in subjects with idiopathic scoliosis. It would be of interest to extend this to

include all involved lumbar levels (Figure 11.2) and the primary thoracic curvature.

While this may pose imaging challenges with respect to MRI slice angles and the

difficulty in obtaining clear mid disc slices the results may be of value in predicting

curve progression and informing management choices.

Page 177: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 11: Conclusions and recommendations

Page XI-8

Figure 11.2: Proposed study examining involved levels beyond the apical segments of

the secondary lumbar curve in scoliosis by applying the same method with mid disc

transect (A), pixel samples across axial slice (B) for analysis of pixel intensity profiles

(C) and determination of NP deformation direction (D).

11.8.3.3 Herniated nucleus pulposus

Application of the described method to subjects with anular rupture and herniated NP

may provide data to inform clinical management of this condition with respect to the

effect of movement and positioning on extruded NP material (McKenzie & May, 2003).

Page 178: NUCLEUS PULPOSUS DEFORMATION IN RESPONSE TO LUMBAR … · ABSTRACT Page i Background The lumbar intervertebral disc (IVD) is comprised of the collagenous anulus fibrosus (AF) and

Chapter 11: Conclusions and recommendations

Page XI-9

References

Adams M, Bogduk N, Burton K, Dolan P. The Biomechanics of Back Pain. London,:

Churchill Livingstone, 2002; p127

Barrett CJ, Singer KP, Day R. Assessment of combined movements of the lumbar spine

in asymptomatic and low back pain subjects using a three-dimensional

electromagnetic tracking system. Man Ther 1999; 4(2): 94-9.

Bogduk N, Lord S. A prospective study centralisation of lumbar and referred pain: a

predictor of symptomatic discs and annular competence: commentary. Pain

Medicine Journal Club 1997; 3: 246-8.

Donelson R, Aprill C, Medcalf R, Grant W. A prospective study of centralization of

lumbar and referred pain: a predictor of symptomatic discs and anular

competence. Spine 1997; 22: 1115-22.

Edwards B. Manual of Combined Movements: Their Use in the Treatment of

Mechanical Vertebral Column Disorders. Edinburgh: Churchill Livingstone,

1992;

McKenzie R, May S. Mechanical Diagnosis and Therapy, 2 ed. Waikanae: Spinal

Publications New Zealand Ltd, 2003;

Singer K, Boyle J, Fazey P. Comparative anatomy of the zygapophysial joints, Grieve’s

Modern Manual Therapy, Edinburgh: Churchill Livingstone, 2004.

Wilke H-J, Kettler A, Claes L. Are Sheep Spines a Valid Biomechanical Model for

Human Spines? Spine 1997; 22(20): 2365-74.