Faculdade de Engenharia da Universidade do Porto

Post-Stroke Postural Control: comprehensive analysis towards more competent prediction and rehabilitation

Maria Carolina Fornari

Thesis Plan

Doctoral Program in Biomedical Engineering

Supervisor: Prof. Dr. João Manuel R. S. Tavares (FEUP)

Co-supervisors: Prof. Dr. Andreia P. Sousa (IPP) / Prof. Dr. Marcos Duarte (UFABC)

2017/2018

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Abstract

The postural control is the basis to any voluntary or automatic movement. This complex

capability establishes reciprocal actions between sensory and motor systems in order to

ensure postural orientation and balance. The balance assessment provides a clue of the

integrity of the communication between the sensory and motor systems, the neural

mechanisms involved in this process, and how the central nervous system processes,

execute and coordinate postural responses. Quantitative posturography, a useful and

very reliable tool, uses a force platform to evaluate the center of pressure (COP), which

is the result of the forces applied to the ground by the human being. The COP is widely

used in scientific and, increasingly, in the clinical practice, and is competent to make an

accurate diagnosis and to follow rehabilitation of stroke patients with postural control

deficits. Stroke is the main cause of long-term disability and causes impairment in

postural control and gait. Furthermore, the posturography variables applied to predict

functional recovery in stroke may be of interest to rehabilitation professionals in order

to help the prognosis and the planning of the treatment. The main purpose of the PhD

project is to contribute to the improvement and consistency of knowledge of the

postural control system of stroke patients and their relevant functional implications such

as gait and activities of daily living. To address these aims, it is proposed to investigate

posturography variables which are used to evaluate the upright quiet stance of healthy

and stroke individuals and to indicate which ones best characterize these populations,

and among them, which would be more appropriate for scientific and clinical

evaluation. Finally, it is expected to demonstrate which of these variables would be

more predictive of the functional recovery.

Keywords: postural control, balance, center of pressure, stroke, gait, prediction,

rehabilitation.

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Content

Chapter 1 ............................................................................................................... 1

Introduction ....................................................................................................... 1

1.1 Motivation ........................................................................................... 2

1.2 Research Goals .................................................................................... 4

1.3 Structure of the document ................................................................... 6

Chapter 2 ............................................................................................................... 8

Postural Control ................................................................................................ 8

2.1 Methods of assessment ...................................................................... 10

2.2 Theories ............................................................................................. 11

2.3 Post-stroke ......................................................................................... 13

Chapter 3 ............................................................................................................. 16

State of the Art ................................................................................................ 16

3.1 Variables of the posturography ......................................................... 16

3.2 Variables of the posturography in stroke ........................................... 18

3.2.1 Other implications ....................................................................... 20

3.3 Prediction in stroke recovery ............................................................. 25

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Chapter 4 ............................................................................................................. 27

Methods ........................................................................................................... 27

4.1 Work package I .................................................................................. 27

4.2 Work package II ................................................................................ 28

4.3 Work package III ............................................................................... 36

4.4 Work package IV ............................................................................... 37

4.5 Timetable ........................................................................................... 38

Chapter 5 ............................................................................................................. 39

Final Remarks ................................................................................................. 39

References ........................................................................................................... 40

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List of figures

Figure 1. World map showing burden of cerebrovascular disease – DALYs

(from [9]). ......................................................................................................................... 3

Figure 2. Location of the 21 reflective markers used to estimate COM and to

investigate the quiet standing kinematics (from Winter el al. [26]). .............................. 32

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Abbreviations and symbols

A/D Analogical-digital

AP Anterior-posterior

BBS Berg Functional Balance Scale

BOS Base of support

CNS Central nervous system

COG Center of gravity

COM Center of mass

COP Center of pressure

COPap COP anterior-posterior

COPml COP medial-lateral

CT Computed tomography

DALYs Disability-adjusted life years

EMG Electromyographic

H-reflex Hoffman reflex

ICC Intraclass Correlation Coefficient

ML Medial-lateral

Mmax Maximum M

MRI Magnetic resonance imaging

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PCA Principal Component Analysis

PST Postural Stress Test

TUG Timed up and go test

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Chapter 1

Introduction

The postural control is a complex ability established on the reciprocal action of

the sensory and motor systems [1, 2]. It uses afferent information from visual, vestibular

and somatosensory receptors to detect and control movements and coordinate reflex and

voluntary muscle responses while ensures stability [3, 4], manages postural orientation

and balance [4].

Impairment or damage in any of postural control related system can disturb

balance or motor activities and increase the fall risks. One of these disorders, with

elevated incidence of falls and high personal and social impact, is the stroke.

Stroke is the main cause of long-term disability in the older population [5].

Although its incidence has decreased in recent decades, the absolute number increases

each year [5], including young adult individuals. Consequently, there is a large

influence on activities of daily life, economics, family, psychological, etc. [5].

Studies suggest that posturography is competent to make an accurate diagnosis

and to follow rehabilitation of stroke patients with postural control deficits [6].

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The posturography uses a force platform to evaluate the center of pressure

(COP), which is the result of the forces applied to the ground by the human being. The

COP is widely used in scientific and, increasingly, in the clinic practice, to evaluate the

postural control of healthy or disabled subjects.

There are many studies in this area, but still, no consensus on which variable

calculated from the COP would best characterize the functioning of the control of

posture and balance [6], especially with alterations caused by stroke.

Studies have shown that patients with stroke have worse stability than healthy

subjects [7], as well as alterations in gait and in the functional activities of daily living.

There is an urgent need to improve the diagnosis, evaluation, and prognosis of

these patients quickly after the stroke, in order to accelerate hospital discharge and the

return to activities of daily living, to avoid the consequences of immobility and hospital

contamination, to reduce expenses and to start soon the rehabilitation process. That is

important to consider that the maximum recovery of these patients occurs within the

first three months after the stroke [8].

1.1 Motivation

The postural control is a relevant scientific and clinical issue because it is an

important requirement for the performance of any voluntary or automatic movement

and functional activities especially gait. However, despite the extensive literature on

biomechanics and neurophysiology of postural control in humans, there is still no

complete understanding.

Extending the study of postural control in individuals with brain lesion and the

comparison with healthy subjects may provide clues to a better comprehension of the

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biomechanical and neurophysiological mechanisms by which the maintenance of the

posture and balance is operated, contribute to the scientific and clinical assessment and

can help the understanding of functional disabilities that occur with some pathologies

such as stroke, as well as assist the right prognosis and more focused treatment.

A few years ago, per thousand people, more than two had suffered from a stroke,

of which 13% died [5]. Although its incidence has declined in recent decades, the

absolute number increases each year, that is, in 2013 there were almost 11 million

people living with stroke sequelae and approximately 1.5 million deaths [5]. From 1990

to 2013, there was a 24.4% increase in the disability-adjusted life years (DALYs), what

represents a major impact on personal life, work productivity, and a financial, economic

and social burden [5] (Figure 1).

Figure 1. World map showing burden of cerebrovascular disease – DALYs (from [9]).

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There were not find many studies in the literature on the quiet upright posture of

stroke patients, principally with a further complete and accurate methodology. Besides,

there is no consensus on which methodology and variables would be most appropriate

in the use of the evaluation of this topic.

The main contribution of this PhD project will be the investigation of

posturography variables never before used in stroke patients (especially COP structural

variables, of which it were found no studies), which will allow further understanding

about the postural control, the mechanisms of neuromotor adaptations caused by

nervous system injury, and the associated functional recovery.

Despite the advances and a large number of studies, the prognosis and

mechanisms of the functional recovery and motor learning after stroke are still not well

established. Additionally, there are few clinical models predictive of motor recovery in

stroke used by rehabilitation professionals.

Accordingly, the posturography variables applied to predict functional recovery

in stroke patients may be of interest to rehabilitation professionals in order to help the

prognosis and the planning of clinical treatment and physical rehabilitation, optimizing

resources, focusing on the real potentials of each patient and appropriate treatment

methods, decreasing anxieties and better instructing the patients, caregivers, and family.

1.2 Research Goals

The main purpose of the PhD project is to contribute to the improvement and

consistency of knowledge of the postural control system of stroke patients and their

relevant functional implications, such as gait and activities of daily living, and

predictive value to motor outcome and recovery.

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To address these aims, it is proposed to conceive four work packages with the

following objectives:

I - A systematic review of the literature on posturography variables calculated

from the COP raw data, which are used to evaluate the upright quiet stance of healthy

and stroke individuals.

II - A cross-sectional study to evaluate the variables related to the upright quiet

stance used in the literature and selected based on the previous study (systematic

review) in healthy and stroke subjects, with the purpose of establishing which ones best

characterize the populations, and among them, which would be more appropriate for

scientific and clinic evaluation.

A statistical analysis, "Principal Component Analysis" (PCA), will be utilized in

order to eliminate the overlaps and determine the most representative data through

linear combinations of the original variables.

The propose is a more comprehensive methodological approach in order to a

more complex and extensive data interpretation and a better understanding of the

associated events with these nervous system tasks. Therefore, four approaches will be

proposed:

(a) to correlate kinetic to kinematic and electromyographic (EMG) variables;

(b) to compare the COP acquisition of the stroke subjects between one and two

force platforms;

(c) to compare the differences in postural control between right and left

hemisphere lesions;

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(d) to investigate the Hoffman reflex (H-reflex) in the upright quiet stance of the

stroke subjects (and to correlate with the biomechanics and neurophysiology involved in

postural control).

III – A reliability analysis of the protocol and variables studied in the works

described above, through "Intraclass Correlation Coefficient" (ICC) [10].

The intrarater and test-retest reliability will be tested (subjects will be

reevaluated after 72 hours of the first collection).

IV – A longitudinal study through the follow-up of stroke patients during the

rehabilitation process. Subjects will be reassessed 1, 3, 6 and 12 months after the first

evaluation. It will be demonstrated which of the investigated variables in the cross-

sectional study (item 2) would be more predictive of the functional gait recovery,

through the correlation with Fugl-Meyer Scale and gait parameters, such as speed,

cadence and limb coordination.

It is intended to correlate the posturography with Magnetic resonance imaging

(MRI) data.

Finally, it is expected to develop a model (or a database) that provides a

prediction of gait recovery in order to support the prognosis and rehabilitation planning

(or a more quantitative and reliable method of assessing postural control and balance for

physiotherapists).

1.3 Structure of the document

The current document has four more chapters:

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Chapter 2, exposes the basic information about the postural control and

assessment methods, particularly in stroke patients.

Chapter 3, relates the state of art of the methodology and variables studied by the

posturography of healthy subjects and with AVE, and clinical predictive models for

motor recovery from stroke patients.

Chapter 4, explains the methodology and procedures that will be used on the

PhD project and related studies. The work packages are comprehensively described and

presented at the timetable.

Chapter 5, presents the final remarks and future expectations.

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Chapter 2

Postural Control

The central nervous system (CNS) coordinates and integrates vital and physical

functions, processes information and provides responses. It receives inputs from many

types of sensory receptors, integrates them with past experiences and other sources,

plans and executes actions. The nerves of the peripheral nervous system communicate

the CNS – cerebral cortex and spinal cord – with the inputs of the different parts of the

body [11].

The cerebral cortex is the major responsible structure for motor control through

the planning, processing and execution of commands. The spinal cord and brainstem

help coordinate reflex and voluntary movements, with the assistance of other

subcortical structures such as the cerebellum and basal ganglia [11, 12].

An essential motor system topic is the postural control, which is the basis to any

voluntary or automatic movement and a complex capability established on reciprocal

action of sensory and motor systems [1, 2]. The postural control is involved in several

subsystems: nervous, sensory, biomechanical and muscular.

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The fundamental aims of postural control are postural orientation and balance [4,

13]. The postural orientation requires the biomechanical alignment of the body and its

position in the environment and its relations with gravity, base of support (BOS), visual

field, internal references, memory, etc. [1, 4]. Balance involves the coordination of

movement strategies to maintain the center of mass (COM) within the BOS during

externally provoked and self-initiated postural disturbances [1, 12].

Postural control uses afferent information from visual, vestibular and

somatosensory receptors to detect and control movements and coordinate reflex and

voluntary muscle responses while ensures stability [3, 4, 14]. Afferent signals are sent

to the cortical motor centers in order to the cortex can be able to process the actual

requests for balance and postural control, and to send efferent signals if was required

[15].

The CNS operates two essential mechanisms to control balance: anticipatory or

proactive mechanisms and compensatory or reactive mechanisms [13].

Anticipatory postural adjustments maintain the postural stability in response to a

predictable disturbance, external – adjustment based on past experience [4] – or due to

voluntary movements [16]. This anticipatory mechanism is related to several factors:

expected magnitude and direction of the displacement, voluntary action associated with

the perturbation, current postural condition, past experiences and practice.

On the other hand, compensatory mechanisms are automatic or reflex responses

to unexpected external disturbances [13] or failures of anticipatory adjustments. These

adjustments are usually extremely fast, and the specific strategy used depends on the

characteristics of the external postural displacement, the individual's expectations and

previous experiences [1].

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This chapter aims to present the postural control theory, associated mechanisms,

and methods of evaluation, its impairments with stroke and the consequences in gait and

functionality.

2.1 Methods of assessment

The balance assessment provides a clue of the integrity of the communication

between the sensory and motor systems because external postural responses quantify

how much the motor system is able to respond to a particular sensory stimulus pattern,

how much the CNS is prepared and adapted for different disturbances, and how well it

is able to learn, execute and coordinate preplanned motor patterns. This evaluation also

allows the inference of the neural mechanisms involved in the process of postural

control, and their coordination to ensure postural orientation and balance.

However, despite the extensive literature on postural control in healthy and

disabled subjects, the assessment of postural adjustments remains difficult to perform

because of the complexity of postural control. Several instruments were developed in

attempt to identify the neural, cortical or subcortical mechanisms underlying this control

[3].

There are simple methods that make predictions of postural stability, as

retropulsion test [17], widely used in clinical practice; the "Postural Stress Test" (PST) –

a more reliable version of the retropulsion test [18, 19]; Berg Functional Balance Scale

(BBS), used to quantify the risk of falls in the elderly [20, 21]; Tinetti test, Mini

Balance Evaluation Systems Test; Timed up and go test (TUG); Unified Balance Scale

and others [1].

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These methods are accessible to any examiner, but they have some

disadvantages, such as the difficulty of reproducibility and standardization for different

masses and heights of the subjects, and they are not useful for the identification of the

physiology involved in the regulation of posture.

Further, these tests are not useful for assessing the performance of any

population since they distinguish only high balance deficits [22].

Currently, more elaborate methodologies have been developed to identify the

influence of sensory inputs and the efficiency of muscle activity in the postural control.

Quantitative posturography, a useful and very reliable tool, uses high technology

to measure ground reaction forces in the BOS by a force platform, EMG and kinematic

patterns and biomechanical analysis related to various motor tasks or to different types

of disturbances [17, 23].

2.2 Theories

Despite the development of sophisticated methods for assessment of postural

control and intense research in this area, there is still no consensus about the

biomechanical and neural mechanisms underlying the control of posture and balance.

The complexity of human postural control is very high due to the involvement of

several subsystems: neural, sensory, biomechanical and muscular.

The literature suggests that neuronal signals sent by stretching or shortening

muscle length alone are insufficient for controlling upright posture [24], consequently,

only a combination of afferent inputs can provide the information necessary to control

body balance [25].

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However, Winter et al. [26] argue that static postural control is maintained only

by the stiffness of the musculoskeletal apparatus. But this statement was debated by

several authors [27, 28].

Morasso et al. [29] indicated that the stiffness of ankle muscles is insufficient to

stabilize the body, suggesting an important role of muscle and sensory receptors foot

plant in controlling human posture. They advocate an anticipatory control of posture

without, however, eliminating the contribution of stiffness of the musculoskeletal

system. They therefore believe in a synergy of these mechanisms.

Presumably, the muscle tonus also contributes to the standing posture [30], but

there is no agreement in the literature about the importance of the active or passive

contribution in the tonus generation.

Some studies shows a dominant role of active mechanisms [25], and others a

predominant contribution of passive mechanisms [31].

Although quiet erect posture could be possible only due to the mechanical

rigidity of the muscles, still, it is verified that the vertical balance is a delicate state. Any

movement of the center of gravity (COG), even if it does not shift the balance is

detected by afferent signals and compensated by the contraction of the postural muscles.

Since all forces in a standing individual are transmitted to the foot, postural reflexes

often involve the contraction of many muscles and are more complex than a simple

stretch reflex [12].

The postural control involves both spinal reflexes and longer loops, more

adaptable and recent phylogenetically related to the motor cortex, brainstem and

cerebellum [11, 12, 25].

Studies indicate that higher cortical structures also play an important role in the

regulation of balance in static and dynamic conditions [32]. It is observed that the

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superior cortical functions related to the posture are linked to the human cognitive

processing. The amount of cognitive processing required for postural control depends

on both the complexity of the postural task and the capacity of the subject's postural

control system [1].

Systems theory suggests that postural control is given by the interaction between

the individual, task and environment, assuming that the ability to control the position of

the body in space comes from the complex interaction between the musculoskeletal and

neural systems [33]. Accordingly with this theory, the maintenance of the quiet upright

posture requires the synergic muscle activation of the two sides of the legs so that the

COM stays within the BOS [34], and there is evidence that this interlimb coordination is

mediated by spinal cord circuits, which are under supraspinal control [35].

The models and theories of postural control have not yet been completely tested

and proven and present many conflicting aspects, so this discussion is still very

vigorous in the scientific community.

2.3 Post-stroke

Studies have shown that patients with stroke have worse stability than healthy

subjects [7], alterations in gait and a greater probability of fall. Several factors may be

associated: biomechanical malalignment, muscle weakness, altered muscle tone and

sensitivity, visual or vestibular deficits, limitations in joint range of motion, emotional

factors as fear of falling, and deficits of attention [5].

In clinical practice, the following changes related to post-stroke postural control

and balance were reported: worse balance stability in the frontal plane, different weight

discharge in the right and left limbs [36], lower efficiency of the postural adjustments,

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stereotyped muscle synergies to disturbances, inadequate muscular activity of lower

limbs and trunk [17, 37-39], and greater difficulty in compensatory adjustments [40].

Many researchers are interested in finding better ways of approaching diagnosis

and treatment of stroke effects that cause equilibrium deficits [2, 41]. The study and

better understanding of the multiple mechanisms underlying the postural control can

help the evaluation of patients with balance deficits, understanding of functional

compensations and effective rehabilitation of balance to improve mobility and prevent

falls.

The results of this study by Rongies et al. [6] indicate that posturography is

competent to make an accurate diagnosis and even to follow the motor and functional

recovery of stroke patients with postural control deficits.

Concerning the posturography, the literature suggests that the lower the area of

postural oscillation (i.e., the amplitude of the area of oscillation of the COP), the better

the control of postural stability [42].

In patients with stroke, many changes were observed in the parameters

associated with the force platform, such as: deviations of the COP to the non-paretic

limb [43], higher frequency of COP oscillation [40], higher COP velocity [44], greater

COP area and amplitude [45, 46], difference in COP amplitude between right and left

lower limbs [47], differences in COP parameters between patients with left and right

hemisphere lesions [48].

Several studies have compared clinical tests with global posturography

variables. Pyoria et al. [36] found correlations between higher velocities of oscillation

with scores in the Functional Standing Balance Scale that indicates equilibrium deficit.

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These disorders in the postural and balance control of stroke patients,

concurrently with other complications, contribute to impairment in gait and

performance of functional activities of daily living.

Although the variations of gait patterns of the stroke patients vary with the

location and extent of the injury, as well as the time after stroke and recovery and

rehabilitation process [49], the literature reports: gait asymmetry, reduced walking

speed, inadequate propulsion of the paretic limb, reduced stance phase and prolonged

swing of the paretic limb, alterations of COM trajectory, synergic patterns of muscle

contraction of the paretic limb, rather than individual control of each joint, more co-

contractions during the stance, among other changes [49, 50].

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Chapter 3

State of the Art

3.1 Variables of the posturography

Many experiments have already been carried out based on the behavior of the

COP and muscular activity in upright static situations [22]. The COP is the point of

application of the resultant of the vertical forces acting on the BOS, and represents a

combined result of the postural control system and the force of gravity. Some authors

consider the COP a response of the CNS to adjust the oscillations of the COM in the

erect posture [38].

It is called posturography or stabilography the measurement and record of the

human postural oscillation.

Static posturography studies the upright quiet posture when the subject tries to

stay without any movements; and the dynamics posturography evaluates the subject's

response when a disturbance is applied [51, 52].

Force platform studies have shown that evoked responses by disturbance provide

excellent examples of the complexity of postural adjustments. Behaviors vary according

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to the instability of the surface and the force of the disturbance. Thus, postural reactions

caused by equilibrium disturbances through different paradigms have been studied [17].

Some of the variables used to examine the behavior of the forces in upright static

posture are areas of trajectory of the COP, velocity and amplitude of displacement,

standard deviation and normalized root mean square.

However, according to a literature review [22], most studies related to the

evaluation of postural control choose techniques, methods, and quantitative variables,

not taking into account the studied population, the goal of the postural task, and the

conditions of the environment.

Usually, raw data of the COP displacement is only used for visual

representations and construction of statokinesigram and stabilogram. It is necessary to

calculate other variables of the COP to intensify the analysis of the mechanisms

involved in the postural system [22].

Global variables are represented by the magnitude of the resultant or

components anterior-posterior (AP) and medial-lateral (ML) of COP (COPap and

COPml, respectively) in terms of time or frequency. Generally, it is considered that

lower the magnitude or deviation of these variables, better the postural stability [22].

The variable considered more reliable and sensitive in the study of postural control is

the velocity of the COP, which reflects the efficiency of the postural control system

[22], and may have a major role in the feedforward mechanisms during quiet stance.

But these variables are not sensitive to other components of COP that could

provide important data to understand the complexity of the functioning of postural

control. Some studies have developed structural variables, which are decomposition of

the COP oscillation patterns, for example, rambling and trembling [53] and fractal

analysis of the COP [22]. Though, these theoretical considerations are not yet entirely

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tested and confirmed. It is still necessary to expand the analysis of all the components

related to the postural control system for the real understanding of its function.

3.2 Variables of the posturography in stroke

Usually the studies about stroke postural control evaluate only some of the

global COP variables.

Wei et al. [7] evaluated, with two platforms, only the standard deviation of the

COPap and COPml displacement of the stroke patients. Rongies et al. [6] only studied

the following variables: COG mean, oscillation amplitude, and area.

In the study of Gasq [54], the variables investigated were: mean and standard

deviation of COP velocity, COPap and COPml mean velocity, area of the 90%

confidence ellipse enclosing COP, absolute value of the mean COPml position, in order

to evaluate the weight-bearing asymmetry. All variables presented a good level of

agreement, except the area and COPml. The area presented low reliability, and the

absolute value of mean COP was not reliable in the study.

The study of Nardone et al. [43] evaluated the postural stability of stroke

patients with a single force platform. Only four variables were evaluated: COPap and

COPml mean position; Area; and COP sway. It has been reported that the area and

length of COP displacement were greater in subjects with stroke than controls, and that

COPml drifted further to the side of the non-paretic limb. But an interesting result was

the correlation between COPml asymmetry and lower limb strength (by the Motricity

index scale). As there was no correlation with spasticity, they conclude that spasticity

alone does not explain the altered balance in these patients, which could primarily be

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explained by alteration of descending cortical signals that control the activation of

motor neurons related to the postural musculature [43].

Gray et al. [44] evaluated the following variables: COP mean velocity, area,

COPap and COPml amplitude. They tested the reliability of the measures with two

force platforms in patients with stroke. The COP mean velocity was the most reliable

variable. They recommend making more than one attempt to improve reliability but

avoid stroke patient fatigue.

Sawacha et al. [55] correlated the following balance tests: Fugl-Meyer, Motricity

Index, Trunk Control Test, Functional Independence Measure, TUG, BBS, and Tinetti

with some COP variables (ellipse, sway area, path and velocity in both directions, AP

and ML). And there were significant differences between healthy and stroke subjects

with open eyes. With closed eyes there was only a difference between parameters

related to COPap and velocity. They argue that CNS post-stroke adapts to maintain the

ML position with eyes closed because of the proprioceptive deficiency, and, therefore,

there was no difference with controls. But in opposition to other studies, they used only

one force platform. They also reported correlations of the tests with a few variables,

showing that clinical tests and posturography evaluate different aspects of the postural

control system [55].

Niam et al. [37], correlated some global variables (COPap and COPml velocity,

RMS velocity, RMS amplitude, COPap and COPml mean frequency) with BBS.

However, only the COPap velocity showed correlation. Their conclusions emphasize

the importance of evaluating the AP and ML directions separately, chose carefully the

parameters, and not use the posturography data alone to make statements [37].

There is, consequently, a requirement of a more comprehensive methodology,

including EMG and kinematic data.

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The study by Roerdink et al. [56] evaluated variables derived from the

dynamical systems, to verify if they add value to the analysis of the conventional

posturography parameters. Among a lot of results and inferences, they reported a

decrease in local stability in stroke patients, which they interpreted as a deterioration of

the neuromuscular control system, and a reduced ability to compensate for minor

disturbances.

They also suggested that the postural system of healthy subjects is more

concerned with the maintenance of the AP balance (which presents greater oscillation

and greater regularity) and the system of stroke subjects is more concerned with the

oscillation in the ML direction [56].

A more comprehensive interpretation could infer that greater oscillation in the

ML direction is due to a greater contribution of the proximal muscles of legs and the

trunk than distal muscles, which are generally more impaired in stroke.

These results corroborate with the importance of EMG evaluation with the

posturography data.

Besides, there was found no agreement in these studies, and there were no

research about COP structural variables in the stroke population.

3.2.1 Other implications

a. Interlimb coordination

An earliest study of Sherrington [57], initiated investigations into interlimb

coordination and demonstrated reflex interconnections between the cervical and lumbar

cat´s cord, that is, between the front and rear limbs during stance and walking. Many

authors have studied spinal cord quadruped coordination [58]; however, it is known that

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the regulation of posture and bipedal gait has fundamental differences, requiring

specific neuronal mechanisms to maintain the body in an upright position.

Among the movements, one of the most studied is certainly the human gait [24],

since the cross responses really have great importance in locomotion. However, few

studies have been found in the literature on interlimb coordination during maintenance

of human orthostatic posture.

Dietz studied spinal cord coordination in humans through displacements in the

quiet erect posture [35]. When only one leg was stimulated, EMG responses for

recovery of balance were very symmetrical in both sides. The minimal movement at the

contralateral ankle joint suggests that these crossed responses come from the displaced

leg signals. However, when contralateral leg is not supporting the body, its muscles

were not activated [35], so they are not connected to a postural program [59].

Short-latency responses are not the same under different conditions: muscle

activation patterns are highly specific for different motor tasks [35].

It was also verified that, after bilateral perturbations in opposite directions, linear

subtraction of EMG responses occurred, that is, activation was induced in the agonist

muscle of one leg and contralateral coactivation in the antagonist - mutual reciprocal

inhibition in the respective antagonists of each activated muscle [35]. The greater the

postural destabilization caused by the disturbance, the greater the degree of muscular

activation. Therefore, lower limbs act synergistically, that is, each limb affects the

activation force and the temporospatial behavior of the other limb.

This coordination between the lower limbs must have a spinal cord origin,

mediated by a few interneurons, because the latencies after the stimulus, approximately

75 to 100 ms, are compatible with propagation in afferents associated with type II

endings of the neuromuscular spindles [35]. Schieppati and Nardone [60] performed a

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series of investigations that point to an important role of type II afferent fibers in the

medium latency component of the human stretching reflex, particularly in the reflex

response of anti-gravity muscles, evoked by disturbances in upright quiet posture.

In addition, no cross excitatory effects from Ia fibers are known in

humans. Disturbances in a single leg do not elicit short latency responses, mediated by

fibers Ia, in the muscles of the undisturbed leg. On the other hand, the medium latency

responses are elicited bilaterally, what is compatible with the hypothesis of the

transmission by type II fibers [60].

Therefore, despite the monosynaptic stretching reflexes do not play an important

role during postural disorders [15], it can be affirmed that afferent feedback and reflexes

have a significant function in the regulation of coordination between members [61].

However, this spinal coordination system, probably mediated by type II afferent

fibers, seems to be under higher influence [35]. The spinal mechanism does not receive

sensory information about body orientation, for instance. Its function is the transmission

of the supraspinal commands about motor patterns of postural corrections. Supraspinal

structures receive information from the vestibular system about orientation of the body

and generate commands for postural corrections [58].

It was reported that, after disturbances of the upright position, patients with

spasticity presented delayed and decreased EMG responses in comparison with healthy

subjects, and the reduction of EMG was correlated with the severity of paresis [62].

There is no evidence that transcortical pathways contribute to the long latency reflexes

observed in lower limbs [15]. Thus, this corroborate with a supraspinal influence on the

spinal reflex pathways. Dietz et al. [15] suggested that the afferent signals are sent to the

cortical motor centers in order to the cortex can be able to process the actual requests

for balance and postural control, and to send efferent signals if was required.

23

The comprehensive analysis of interlimb coordination of the stroke individuals

in association with the investigation of the reflex pathways, through the measurement

and analysis of H-reflex during the maintenance of quiet standing posture, could

provide clues about neurophysiological mechanisms involved in the control of posture

and the dysfunctions occurring in the nervous system with brain injury (approach ‘d’ of

work package II).

Dickstein and Abulaffio [63] evaluated the coordination between hip and leg

oscillation and between the paretic and non-paretic limbs of stroke patients and control

subjects. An asymmetry was found between limbs in the patients, with greater

oscillation in the paretic limb. They also found a synchronization deficit between the

movements of the hips and legs of the same limbs of the patients. It has been reported a

correlation between the oscillation of the hips of both limbs but not of the legs,

suggesting a more pronounced deficit in stabilizing more distal segments in the paretic

leg of these patients, as verified in clinical practice. Nevertheless, they did not correlate

these data with posturography data.

A study by Wei et al. [7] has shown that patients with stroke have poorer

coordination between members in the AP direction. Notably, the coordination between

members improves with the eyes closed perhaps because the system tries to compensate

the absence of an important sensory afferent. They also found greater oscillation in the

non-paretic leg than the paretic, but did not correlate these data with muscle activation.

They suggested that the system attempts to maintain equilibrium by increasing the

adjustments in the non-paretic limb, and therefore, a greater oscillation demonstrates a

greater CNS action [7]. However, this result could be due to a decrease of the muscular

activity by the injury in the cortex motor area.

24

The comparison of COP behavior between one and two force platforms, with

EMG and kinematic data, can provide valuable information for the comprehension of

interlimb coordination in stroke quiet standing (approaches ‘a’ and ‘b’ of work package

II).

b. Differences between lesions in the left and right hemispheres

Another important question is about the sample of evaluated stroke patients,

which is always highly heterogeneous.

Fernandes et al. [48] compared postural control of hemiparetic patients on the

right and left. Although patients exhibited similar scores in clinical tests, patients with

right hemisphere lesions presented bigger changes in posturography data compared to

patients with a left lesion, in accordance with others studies [37, 64]. Since they did not

find a correlation in the sensory system manipulations (without vision and alteration in

proprioception) between healthy subjects and patients, it was suggested that this

alteration would not be explained by a specialization of the right hemisphere in

somatosensory processing, but by a change in the generation of descending responses.

Thus, the right hemisphere would be more specialized in maintaining the quiet posture

(which requires small adjustments of the body to maintain balance).

It has been suggested that these adjustments would be related to muscle intrinsic

stiffness and viscosity [48].

From these data, it will be interesting to evaluate the stiffness in the quiet upright

posture in the stroke population. The stiffness can be calculated from kinematic data,

according to the methodology of Winter et al. [26].

They also argue that there was no difference in muscle activation of the non-

paretic leg of patients compared to healthy subjects, but it was not concluded whether it

25

is a normal activation or CNS recovery process (to compensate for paretic leg deficit)

[48]. The literature suggests that the ipsilateral limb to the lesion would also suffer

deficits through uncrossed neural pathways [49]. This could be tested by comparing

patients with acute and chronic stroke.

Considering that the brain lesions caused by stroke are always very specific and

in different locations, it is necessary a better characterization of these subjects and a

separation between two groups: the patients with right and with left lesion (approach ‘c’

of work package II).

3.3 Prediction in stroke recovery

Predicting motor recovery, despite being better known in medical practice, is

still limited adopted or not well understood by physiotherapists [65, 66].

There are many tools for clinicians described in the literature and used in clinical

practice, however, the quantity and application of instruments that can guide or predict

the prognosis and assist in the planning of an effective and optimized treatment is still

very limited in physiotherapeutic practice.

This study by Eghidemwivbie and Schneeweis [67] has shown that

physiotherapists are able to make predictions about the outcome of walking and daily

living activities, and that this prediction is extremely useful in determining the treatment

plan and orientation to the patients and their relatives. The earlier this prediction is

made, the results tend to be more accurate. However, there is a lack of tools to assist or

guide this process, and it is recommended to use statistical models for appropriate

prognosis and treatment plans [67].

26

The result of a systematic review has suggested that neuroimaging data may be

useful in predicting motor recovery of upper limbs, but there is no strong evidence that

models with such data are better than models with clinical data or that adding

neuroimaging data improves such prediction [68]. Besides, to date, none of the

prediction models for walking have been validated [68].

The meta-analysis of Fahey et al. [39] did not identify any impact assessment

study, as randomized follow-up or cross-sectional, or any of the study assessments of

utility, such as decision curve analysis. However, more than half of the models included

in this review would need studies that focus on additional validation using different

external cohorts, improving the accuracy reported by refinement models, and

significantly evaluating the impact of models in the clinic.

Those who wish to predict the outcome of stroke are advised to build on

previous work, to update and adapt validated models to their specific contexts rather

than to build new models. Although this study identified precise predictive risk factors

for mortality and recovery, its usefulness remains uncertain [39].

27

Chapter 4

Methods

The following will describe in detail the methodologies that will be applied to

achieve the objectives described in chapter 1, namely: a systematic review, cross-

sectional study, reliability study, and longitudinal study.

4.1 Work package I

A systematic review will be divided into two parts:

The first one will review and study the papers about posturography variables

used to evaluate the upright quiet stance in healthy individuals.

A search will be performed on the databases: MedLine, ISI Web of Sciences,

and Scopus. The following keywords will be used:

((postural AND control) OR balance OR posture OR standing) AND ((upright

OR orthostatic) AND quiet) AND (posturography OR stabilography OR (force AND

platform) OR (center AND pressure) OR COP).

28

The second review will be about the variables used to investigate the postural

control of stroke patients. The same databases will be used for searching. To the

keywords will be added "stroke":

stroke AND ((postural AND control) OR balance OR posture OR standing)

AND ((upright OR orthostatic) AND quiet) AND (posturography OR stabilography OR

(force AND platform) OR (center AND pressure) OR COP).

Only articles that evaluate the upright quiet stance, in force platform (and not

other devices) in healthy subjects, without any pathology, will be selected.

The following criteria of inclusion will be established: 1) the study must be

written in English; 2) studies with different main focus will be excluded.

4.2 Work package II

This second study will be the experimental analysis of the COP variables.

Subjects

It will be made a statistic approach, to determine the minimum quantity of the

sample of the acute stroke subjects necessary to reliable results.

The stroke subjects will be divided into two groups: patients with right

hemisphere lesion and patients with left hemisphere lesion (verified by computed

tomography – CT – or MRI).

A group of control subjects with matched age, weight and height will be

evaluated for comparison.

29

For the selection of patients and data collection, some agreements will be made

with institutions, namely Centro de Estudos de Movimento e Actividade Humana da

Escola Superior de Tecnologia da Saúde do Instituto Politécnico do Porto, Centro de

Reabilitação Profissional de Gaia, Hospital São João. Other laboratories and clinical

centers will be considered if necessary.

The inclusion criteria for the group of patients will be: (1) hemiparesis due to a

first ischemic stroke in the territory of the middle cerebral artery visualized by CT or

MRI; (2) have the ability to stand without assistance, but with supervision if necessary.

The exclusion criteria will be: (1) cognitive deficits that prevent understanding

and cooperation in the tests (evaluated by the Mini Mental State Examination); (2)

history of orthopedic or neurological disorders (other than stroke); (3) history of stroke

involving the brainstem or cerebellar areas; and (4) taking medications that may affect

motor performance.

As selection criteria for the control group, it will be necessary that the individual

does not present antecedents or current history of neurological pathologies or articular

deformities.

The project will be submitted to the Ethics Committee of the Instituto

Politécnico do Porto, in accordance with the Declaration of Helsinki. All subjects will

sign an informed consent form to participate in the experiments.

Local

The experiments will be performed in the Centro de Estudos de Movimento e

Actividade Humana da Escola Superior de Tecnologia da Saúde do Instituto

Politécnico do Porto.

30

Materials and equipment

Force Platform

Two force platforms, model FP4060-10 from Bertec Corporation (USA),

connected to a Bertec AM 6300 amplifier, with default gains, and at 1000 Hz sampling

rate, will be used. The amplifier will be connected to a Biopac 16 bit analogical-digital

(A/D) converter from Biopac Systems, Inc. (USA).

EMG

For the EMG activity will be used the model MP 100 Workstation from Biopac

Systems, Inc. (USA), with a sampling rate of 1000 Hz and an amplified band-pass filter

between 10-500 Hz.

Data will be collected using steel electrodes, model TSD150 from Biopac

Systems, Inc. (USA), bipolar configuration, with an 11.4 mm contact area and an inter-

electrode distance of 20 mm, and a ground electrode.

Prior to the placement of the electrodes, the skin will be cleaned with 90%

alcohol and prepared with an abrasive solution. The electrodes will be firmly fixed with

an anti-allergic tape, and an electrolytic gel will be used to contact the skin. The skin

impedance will be measured and should have a maximum of 20 kΩ.

The following convention [69] will be adopted for the positioning of the

electrodes in the muscles (both sides), reported in the literature with an important role in

maintaining the posture:

Tibialis Anterior, 1/3 on the line between the tip of the tibia and the tip of the

medial malleolus;

31

Soleus, 2 cm distal to the lower border of the medial gastrocnemius muscle belly

and 2 cm medial to the posterior midline of the leg;

Medial Gastrocnemius, most prominent bulge of the muscle;

Rectus Femoris, 1/2 on the line from the anterior spina iliaca to the superior

border of the patella;

Vastus Medialis, 4 cm above the patella upper border and 3 cm measured

medially and oriented 55º to a reference line drawn between the right anterior-superior

iliac spine and the patella center;

Biceps Femoris, 1/2 on the line from the ischial tuberosity and the lateral

epicondyle of the tibia;

Rectus Abdominis, 3 cm to the right of the umbilicus;

Erector spinae, 2 finger width lateral from the spinous process of L1.

Video Cameras

The software Qualysis Track Manager will capture video from seven high speed

cameras.

Twenty-one reflective markers will be placed on the legs, thighs, lower arms,

upper arms, pelvis, and trunk, according to Winter et al. [26], because this is the

approach to calculate the stiffness, one variable of interest in this work (Figure 2).

32

Figure 2. Location of the 21 reflective markers used to estimate COM and to investigate the quiet standing

kinematics (from Winter el al. [26]).

Procedures

The stroke patients will be evaluated with the Fugl-Meyer Assessment by a

trained physiotherapist.

Then, in the orthostatic posture, the EMG surface electrodes will be placed on

the subject, and then the reflective markers will be attached at the mentioned anatomical

points above.

First, the subject will stand on one force platform, with the two feet, assuming a

quiet upright stance with the feet positioned as comfortable as possible. The anterior

33

and lateral limits of the feet shall be demarcated with adhesive tape so that the

individual returns to the same position in subsequent trials.

The subject will be asked to remain in the orthostatic position as still as possible

for 60 s. There will be three trials with open eyes and three trials with eyes closed.

Between each trial, there will be a rest period of two minutes. When the subject

stands up, there will be a period of 10 to 15 s in order to stabilize before starting each

acquisition.

Two force platforms

Second, the subject will stand on two force platforms with one foot in each one.

The anterior and lateral limits of the feet shall be demarcated again, and the same

instructions and protocols will be performed.

Gait analysis

Following another rest period, all subjects will be required to walk, with a

preferred speed (self-selected), for 10 m along a force platform located in the middle of

the walkway. The subjects will be barefoot and will look forward, walking as naturally

as possible. There will be a previous practice in order that only one foot at a time have

full contact with the platform, and there will be no extra pressure of any other kind on

the platform [70].

H-reflex

Another group of stroke patients will be selected for the H-reflex approach in

order to avoid fatigue. The subject characteristics and inclusion/exclusion criteria will

be the same described above.

34

The tibial nerve will be stimulated with an electrical stimulator MEB 4200, by a

surface electrode with a cathode of 5 mm diameter, fixed to both legs, in the popliteal

fossa. The anode will be attached on the patella.

The stimulus intensity will be determined for each leg that causes an H-reflex

amplitude equal to about 20% of the corresponding maximum M (Mmax) amplitude

response. All trains of stimuli used in the experiments will be at 1 Hz. The electrical

stimulation will follow the model used to capture the reflex of the soleus described by

Mezzarane & Kohn [71].

The subjects will be positioned in the sitting posture with the lower limbs in

extension supported in a seat (no knee flexion will be allowed during the experiment in

order to avoid displacement of the stimulation electrode). In this position, the Mmax

wave of the soleus muscle will be determined through pulses of 1 ms duration. It will be

selected a current intensity which can evoke an H wave of 20% of the Mmax wave.

As in the above protocol, the subject will stand on two force platforms. The

anterior and lateral limits of the feet will be demarcated.

The subject will be asked to remain in the orthostatic posture as still as possible

for 60 s. Around the 20 s of acquisition, a moment unknown to the subject so that he

does not anticipate any reaction, the experimenter will release an electrical stimulus of

the determined intensity. After the stimulus, the acquisition will be completed with a

total time of 60 s. Then, the subject will be asked to sit in a comfortable armchair for 2

min rest. The amplitude of the H wave will be measured in real time.

The experiment will be replicated as many times as necessary so that three

acquisitions are obtained in which the value of the H-reflex amplitude is equal to that

determined value. Three acquisitions will be recorded with eyes open and three with

eyes closed.

35

Analysis of the results

After the conclusion of the trials, the acquisition of the maximum voluntary

contraction of all muscles bilaterally, for normalization of the EMG signals, will be

performed [72].

Subjects will be encouraged to perform maximum force through verbal stimuli

of the experimenter. Only after the beginning of the activity by the subject, the

experimenter will begin the collection. It will be collected 5 s of EMG and saved in the

DataWave environment. For the estimation of the CVM, a time window will be taken

from the middle of the captured period, since the data are more constant, and therefore,

more reliable in this interval.

The signals will be recorded on the personal computer and converted to a text

file so that they can be evaluated via the Matlab software, which will be used for all

tasks of signals visualization and processing and graphics production.

The EMG signals will be normalized, rectified and filtered so that the

observation of the patterns of the muscular activities is facilitated.

The platform signals will be calibrated and converted into units of force

(Newton) and moments of force (Newton x meter). The COP on the foot surface will be

calculated from them, although in this research it will also be included in the analysis

the basic variables provided by the platform (forces and moments), which may help for

a better understanding of the mechanisms involved.

The images of the cameras will be paired with the EMG and the force platform

signals.

The gait data will be used in work package IV.

36

Firstly, the various captured and processed signals will be evaluated individually

for each subject and their mean and standard error will serve to characterize the

individual and its intrinsic variability. In the set of individuals, an analysis of inter-

subject variability will be made.

Comparisons will be made between the three groups (right stroke, left stroke,

and control), between the data from one and two force platforms, and between the

paretic and non-paretic leg of the stroke subjects. Correlations between the kinetic,

EMG and kinematic data will be performed.

A statistical procedure, PCA, will be performed to eliminate the overlaps and

determine the most representative data through linear combinations of the original

variables of the groups.

The statistical analysis will be performed in the Minitab environment with a

significance level of 0.05.

4.3 Work package III

The evaluated variables in the work package II will be tested for reliability.

For this, the subjects will be assessed 72 hours after the first evaluation, with the

same protocol.

A statistical treatment of concordance analysis will be done through the ICC

procedure.

The statistical analysis will be performed in the Minitab environment with a

significance level of 0.05.

37

4.4 Work package IV

The procedure of the work package II will be replicated in stroke group after 1,

3, 6 and 12 months.

It will be verified which variables would be predictive of motor recovery

through:

- the collected posturographic data will be correlated with the Fugl-Meyer score.

- correlation between the gait parameters, such as (speed, cadence and limb

coordination) and posturography.

An attempt will be made to create a model or program that will assist in

evaluation, prognosis, and treatment plan of the stroke patients.

38

4.5 Timetable

Work package I Work package II Work package III Work package IV Thesis

Systematic review Cross-sectional study Reliability analysis Longitudinal study

2018 2019 2019 2020 2020

JUL AGO SET OUT NOV DEZ JAN FEV MAR ABR MAI JUN JUL AGO SET OUT NOV DEZ JAN FEV MAR ABR MAI JUN JUL AGO SET OUT NOV DEZ

Literature review

Reading Writing

Variable analysis

Writing

Variable analysis

Writing

Variable analysis

Writing

Thesis writing

Ethics Committee

First data collection

Data processing

Ethics Committee

First data collection

Data processing

X

Data collection Data

processing

39

Chapter 5

Final Remarks

In this PhD project, it is intended to settle a posturographic protocol that could

be used in the evaluation of the postural control in both healthy or disabled individuals,

highlighting which the variables calculated from raw COP data would best characterize

and discriminate different populations or tasks in an upright postural, such as quiet

standing.

The second expectation is to create a tool, from the posturography data, for

evaluation and prediction of the motor recovery of patients with stroke, which, in the

future, could be extended to other pathologies or contexts.

40

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