5
Vascular accidents after neck manipulation: cause or coincidence? On this background, a formal assessment of the nature of the association against Hill’s time-tested criteria of causation (9) seems appropriate. Hill’s criteria The statistician Austin Bradford Hill (1897–1991) is credited with listing the minimal conditions which are required for establishing that an association (e.g. manipulation and stroke) is causal by nature (e.g. manipulation causes stroke) (9). His nine criteria are well established and form the basis for evaluating cau- sality in many areas of research. In the following, I will apply them to the question whether vascular accidents after neck manipulation are cause or coincidence. Temporal relationship Hill’s first criterion states that the exposure must always precede the outcome. With spinal manipula- tion, this seems to be the case. In all instances, patients first received the treatment and subsequently fell ill (1). However, the situation might be more compli- cated than that. Vertebral arterial dissection can have multiple causes and many predisposing factors have been considered (10). Patients with spontaneous arterial dissection frequently experience headaches and neck pain (11) in the course of their condition. These symptoms could therefore be the very complaints that bring such patients to consult a chiropractor or other therapists applying manipulative therapy. In this scenario, the exposure to neck manipulation would not have occurred before but after the outcome (12–16). In the follow- ing, I will refer to this alternative pos- sibility as ‘the theory of pre-existing pathology’. A recent case–control study seems to support the theory of pre-existing pathology (17). In this retrospective analysis, the risk of a stroke proved to be significantly increased after con- sulting a chiropractor, but not more than so after seeing a primary care physician. Therefore, these authors concluded that the increased risk of a stroke ‘is likely due to patients with headache and neck pain from verte- brobasilar artery dissection seeking care before their stroke’ (17). Unfortunately, this analysis has several important weaknesses and its conclusions are thus less than compelling (18). This study disagrees with an earlier case–control study, in which rigorous attempts were made to control for the possibility of pre-existing symptoms. The conclusion was that spinal manipula- tion ‘is independently associated with vertebral arte- rial dissection, even after controlling for neck pain’ (19). Many cases of vascular accidents occur suddenly and directly after neck manipulation (1,4,20–27) (Table 1). Patients with connective tissue abnormali- ties may be particularly prone to cervical artery dissection (28). A retrospective analysis showed that 63% of all cerebrovascular accidents happen immedi- ately after spine manipulation (29). If it was true that the dissection precedes the treatment, one would not necessarily expect such an immediate onset of symp- toms after spinal manipulation. Therefore, many clinicians observing and reporting these vascular accidents deem causality likely or even certain (e.g. 30). Considering the totality of this evidence, it seems probable that neck manipulation often precedes vascular accidents. In some instances; however, manipulation might also exacerbate a pre-existing dissection. Indeed, Smith et al. (19) published a case where this course of events is well-documented his- tologically in a patient who died after neck manipu- lation. Both of these scenarios would mean that manipulation is causally related to the outcome – Vascular accidents, including strokes and deaths, after upper spinal manipulation are a well-recognised problem (e.g. 1,2). Underreporting of such events renders the calculation of reliable incidence rates impossible (3,4). Most vascular accidents are because of vertebral artery dissection which, of course, can also occur spontaneously in predisposed individuals (e.g. 5,6). Therefore, the nature of the association between spinal manipulation and vascular accidents is uncertain and has been hotly disputed for many years. Some proponents of chiropractic seem to believe that even the critical evaluation of the evidence amounts to a ‘scare story’ (Chairman of the UK General Chiropractic Council) (7) or to ‘puffing up (the evidence) out of all proportion’ (President of the British Chiropractic Association) (8). PERSPECTIVE ª 2010 Blackwell Publishing Ltd Int J Clin Pract, May 2010, 64, 6, 673–677 doi: 10.1111/j.1742-1241.2009.02237.x 673 Many cases of vascular accidents occur suddenly and directly after neck manipulation

Vascular accidents after neck manipulation: cause or coincidence?

  • Upload
    e-ernst

  • View
    223

  • Download
    3

Embed Size (px)

Citation preview

Page 1: Vascular accidents after neck manipulation: cause or coincidence?

Vascular accidents after neck manipulation:cause or coincidence?

On this background, a formal assessment of the

nature of the association against Hill’s time-tested

criteria of causation (9) seems appropriate.

Hill’s criteria

The statistician Austin Bradford Hill (1897–1991) is

credited with listing the minimal conditions which are

required for establishing that an association (e.g.

manipulation and stroke) is causal by nature (e.g.

manipulation causes stroke) (9). His nine criteria are

well established and form the basis for evaluating cau-

sality in many areas of research. In the following, I will

apply them to the question whether vascular accidents

after neck manipulation are cause or coincidence.

Temporal relationshipHill’s first criterion states that the exposure must

always precede the outcome. With spinal manipula-

tion, this seems to be the case. In all instances, patients

first received the treatment and subsequently fell ill

(1). However, the situation might be more compli-

cated than that. Vertebral arterial dissection can have

multiple causes and many predisposing factors have

been considered (10). Patients with spontaneous

arterial dissection frequently experience headaches and

neck pain (11) in the course of their condition. These

symptoms could therefore be the very complaints that

bring such patients to consult a chiropractor or other

therapists applying manipulative therapy. In this

scenario, the exposure to neck manipulation would

not have occurred before but after

the outcome (12–16). In the follow-

ing, I will refer to this alternative pos-

sibility as ‘the theory of pre-existing

pathology’.

A recent case–control study seems

to support the theory of pre-existing

pathology (17). In this retrospective

analysis, the risk of a stroke proved to

be significantly increased after con-

sulting a chiropractor, but not more

than so after seeing a primary care

physician. Therefore, these authors

concluded that the increased risk of a

stroke ‘is likely due to patients with

headache and neck pain from verte-

brobasilar artery dissection seeking

care before their stroke’ (17).

Unfortunately, this analysis has several important

weaknesses and its conclusions are thus less than

compelling (18). This study disagrees with an earlier

case–control study, in which rigorous attempts were

made to control for the possibility of pre-existing

symptoms. The conclusion was that spinal manipula-

tion ‘is independently associated with vertebral arte-

rial dissection, even after controlling for neck pain’

(19).

Many cases of vascular accidents occur suddenly

and directly after neck manipulation (1,4,20–27)

(Table 1). Patients with connective tissue abnormali-

ties may be particularly prone to cervical artery

dissection (28). A retrospective analysis showed that

63% of all cerebrovascular accidents happen immedi-

ately after spine manipulation (29). If it was true that

the dissection precedes the treatment, one would not

necessarily expect such an immediate onset of symp-

toms after spinal manipulation. Therefore, many

clinicians observing and reporting these vascular

accidents deem causality likely or even certain (e.g.

30).

Considering the totality of this evidence, it seems

probable that neck manipulation often precedes

vascular accidents. In some instances; however,

manipulation might also exacerbate a pre-existing

dissection. Indeed, Smith et al. (19) published a case

where this course of events is well-documented his-

tologically in a patient who died after neck manipu-

lation. Both of these scenarios would mean that

manipulation is causally related to the outcome –

Vascular accidents, including strokes and deaths, after upper

spinal manipulation are a well-recognised problem (e.g. 1,2).

Underreporting of such events renders the calculation of

reliable incidence rates impossible (3,4). Most vascular

accidents are because of vertebral artery dissection which,

of course, can also occur spontaneously in predisposed

individuals (e.g. 5,6). Therefore, the nature of the association

between spinal manipulation and vascular accidents is

uncertain and has been hotly disputed for many years. Some

proponents of chiropractic seem to believe that even the

critical evaluation of the evidence amounts to a ‘scare story’

(Chairman of the UK General Chiropractic Council) (7) or to

‘puffing up (the evidence) out of all proportion’ (President of

the British Chiropractic Association) (8).

PERSPECT IVE

ª 2010 Blackwell Publishing Ltd Int J Clin Pract, May 2010, 64, 6, 673–677doi: 10.1111/j.1742-1241.2009.02237.x 673

Many cases

of vascular

accidents

occur suddenly

and directly

after neck

manipulation

Page 2: Vascular accidents after neck manipulation: cause or coincidence?

either as the main cause or by precipitating a vascu-

lar accident to which the patient was predisposed.

StrengthStrength is defined as the size of the association. The

fact that, underreporting (4) several hundred cases of

vascular accidents after spinal manipulation is on

record (1) seems to indicate that the strength of this

association is considerable. The risk of a vascular

accident with, as opposed to without, exposure to

neck manipulation within a week was significantly

elevated (odds ratio = 5, 95% CI = 1.32–43.87) (31).

This is indicative of a strong association.

The strength of the association could also be sup-

ported by other types of evidence. For instance, upper

spinal manipulation has been associated with a range

of injuries other than arterial dissection (Table 2)

(32,25,33–41); all or most of which do not occur

spontaneously. Similarly, spinal manipulations of the

thoracic and lower spine have also been associated

with traumatic injuries (42), and bilateral vascular

injuries have been reported after neck manipulations

(43,44). The totality of this evidence seems to indicate

that there is a strong link between the physical force of

the manipulation and mechanical damage of anatomi-

cal structures at the sites where that force was applied.

Dose–response relationshipThe nature of arterial dissections means that this event

is a ‘yes or no response’. Therefore, a typical dose–

response relationship is not to be expected. However,

there may be a different type of dose–response

relationship. Osteopaths and chiropractors see patients

with similar conditions. Chiropractors frequently use

the type of neck manipulation (high-velocity, low-

amplitude thrusts with a rotational element) that

might cause vascular accidents, while osteopaths tend

to prefer soft tissue techniques (mobilisation) and

employ the implicated techniques less frequently (45).

Vascular accidents are associated much more

commonly with chiropractors than with osteopaths.

One systematic review, for instance, listed 22 patients

of vascular accidents after chiropractic treatment and

found not a single case of such an event after

osteopathic treatment (1). Thus, there may be a dose–

response relationship in so far, as more frequent use of

the suspect type of neck manipulation is associated

with more vascular accidents.

ConsistencyAn association is consistent if results are confirmed

in different settings and with different types of

investigations. The association between spinal manip-

ulation and vascular accidents has been reported in

case reports, retrospective analyses, surveys and case–

control studies from across the world (1). A system-

atic review of the possible risk factors for cervical

artery dissection included 31 case–control studies.

Strong associations were reported from individual

studies for several risk factors for cervical artery

Table 1 Quotes from published case reports

First author (ref) Quote

Donzis (21) ‘… immediately after the initial adjustment of her cervical spine region… (the patient) has lost most of her left

peripheral visual field’

Jones (22) ‘During one of her visits, rapid rotational neck manipulation produced severe head and neck pain followed by

bilateral blindness’

Hillier (23) ‘Immediately after this procedure (sudden lateral flexion adjustment) the patient began to feel vaguely unwell…’

Garner (24) ‘The change in vision began during chiropractic manipulation of this cervical spine’

Chung (25) ‘Immediately [after sudden and forceful rotational neck manipulation] the patient developed numbness of the

whole body and difficulty breathing’

Vibert (26) ‘Immediately after an abrupt rotational head movement, she experienced a severe rotary vertigo with nausea

and vomiting’

Yokota (27) ‘A 38-year-old man suddenly developed nausea, vomiting and vertigo during chiropractic manipulation’

Vascular

accidents are

associated

much more

commonly with

chiropractors

than with

osteopaths

Table 2 Examples of other types of injuries associated

with spinal manipulation

First author (ref) Type of injury

Lipper (32) Cord hemisection

(Brown-Sequard Syndrome)

Chung (25) Cervical cord injury

Tseng (33) Cervical epidural haematoma

Segal (34) Cervical epidural haematoma

Tolge (35) Phrenic nerve palsy

Schram (36) Phrenic nerve palsy

Padua (37) Myelopathy and radiculopathy

Schmitz (38) Cervical fracture

Chen (39) Haematoma of cervical ligamentum flavum

Tome (40) Multiple cervical disc herniations

Tseng (41) Rupture of cervical disc

674 Perspective

ª 2010 Blackwell Publishing Ltd Int J Clin Pract, May 2010, 64, 6, 673–677

Page 3: Vascular accidents after neck manipulation: cause or coincidence?

dissection. These included ‘trivial trauma in the form

of manipulative therapy of the neck (odds ratios: 3.8;

95% CI, 1.3–11)’ (46). It follows, I think, that the

criterion of consistency is fulfilled.

PlausibilityThe association between neck manipulation and

vascular accidents is in agreement with our under-

standing the pathophysiology of vascular incidents:

hyper-extension and ⁄ or rotation of the upper spine

beyond the physicological range puts a pathological

strain on the vertebral artery which, in predisposed

individuals, may result in intimal tearing.

Dissection occurs most commonly at the level of

the atlantoaxial joint. This intimal injury can be

followed by intra-mural bleeding or pseudoaneurism

formation, which can result in thrombosis, embolism

or arterial spasm (43,27). Direct evidence using sin-

gle photon emission tomography in healthy volun-

teers demonstrated that cerebellar hypoperfusion

does occur because of neck manipulation (47).

Here, we must also critically assess the plausibility

of the theory of pre-existing pathology (see above).

Vascular accidents after neck manipulation have been

reported even if the presenting symptom was not neck

pain or headache (48), for instance, in patients who

consulted a chiropractor for back pain (22), scapulagia

(26), torticollis (48), abdominal complaints (48),

scoliosis (48), head colds (48) or hay fever (48). None

of these complaints is symptoms or signs of a

pre-existing arterial dissection. As already mentioned,

vascular accidents have been associated mostly with

chiropractors rather than osteopaths (1). Osteopaths

also frequently treat neck pains and headaches, but

they use high-velocity, low-amplitude thrusts (the type

of neck manipulation implicated) far less than

chiropractors (45). Thus, the association seems to exist

between extreme neck manipulation and vascular

accidents rather than between treating neck pain ⁄headache and vascular accidents. These facts would

seem to considerably decrease the plausibility of the

theory of pre-existing pathology and increase therefore

the plausibility of a causal relationship between neck

manipulation and vascular accidents.

Other explanationsAs discussed above, arterial dissection can occur

spontaneously (11). Therefore, an alternative expla-

nation does usually exist.

Experimental confirmationAs the vertebral artery becomes the basilar artery

entering the base of the skull, it bends sharply from

a vertical to a horizontal path. At this point, the

artery is vulnerable to injury from rotation and

hyper-extension (49–51). Neck manipulation can

decrease cerebellar blood flow (47) and blood flow

velocity in the vertebral artery (52–54). Cadaveric

studies have shown that, during cervical rotation,

stretching, compression and kinking can occur (55).

The consequences can be vasospasm (56) as well as

vascular lesions such as endothelial rupture, ruptures

of the entire vascular wall and intra-mural haema-

toma (57–60). In turn, these events would lead to

ischaemic brain damage (59,56,61). Hypoplasia of

the vertebral arteries or osteophytes of the cervical

vertebrae may predispose to such events occurring

after spinal manipulation (62–64).

Yet the situation is not without contradictions.

Cadaveric studies have suggested that neck manipula-

tion is ‘very unlikely to mechanically disrupt the verte-

bral artery’ (65). However, the validity of cadaveric

studies to the situation in vivo might be questioned,

and the findings await independent replication.

SpecificityThere are, of course, numerous possible causes for

arterial dissections other than neck manipulations

(e.g. 11,17). Therefore, the association is not specific

in the usual sense. However, a different kind of

specificity can be noted: vascular accidents occur

specifically after cervical (rotational) spinal manipu-

lation and not after manipulation to other regions of

the spine (66–70). During rotational manipulation,

the vertebral artery is stretched, compressed and

torqued (10). Cadaveric, electromagnetic flow metre,

angiographic resonance studies have shown that

rotation of the neck decreases blood flow, in the

vertebral arteries (55,71,72,52,53), and 87% of all

vascular accidents after chiropractic manipulations

are associated with neck rotation (10). If the theory

of pre-existing pathology was correct, vascular acci-

dents in people without a predisposition to arterial

dissection should happen after spinal manipulation

regardless of the region treated.

CoherenceCoherence describes the need for any causal associa-

tion to be compatible with existing theory and

knowledge. Accepting that manipulation can cause a

vascular accident would certainly not contradict any

accepted theory or knowledge. Considering also the

bulk of above arguments, the criterion of coherence

seems to be fulfilled.

Conclusion

Thus, only one of Hill’s nine criteria for causality is

not fulfilled: other explanations (criterion No. 6). All

other criteria are at least partly fulfilled. It follows

Causality

between neck

manipulation

and vascular

accidents is

not absolutely

certain but

very likely

Perspective 675

ª 2010 Blackwell Publishing Ltd Int J Clin Pract, May 2010, 64, 6, 673–677

Page 4: Vascular accidents after neck manipulation: cause or coincidence?

that causality between neck manipulation and vascu-

lar accidents is not absolutely certain but very likely.

This notion also seems to be confirmed by clinical

experience; in a review of 32 patients’ reports, causa-

tion was deemed ‘certain’ in 6 and ‘likely’ in 17

patients (1).

Even if one took a different view, and many chiro-

practors will disagree with my interpretation of these

data, the fact remains that causality cannot be ruled

out. Applying the precautionary principle, this would

mean that, until compelling data to the contrary are

available, neck manipulations should be seen as

causing serious adverse events. Another argument

could be the notion that vascular accidents after spinal

manipulation are extreme rarities. The estimates for

incidence vary between 1 per 40,000 and 1 per

1,000,000 cervical manipulations (48). But even if we

concede that they are rare, considering the lack of

conclusive evidence for the effectiveness of neck

manipulations (73), it would seem unwise to recom-

mend this form of treatment; a risk-benefit analysis is

not positive.

While some experts have called for a ban in neck

manipulation (e.g. 74), I would agree with the view

voiced more than a decade ago: ‘the indication for

chiropractic manipulation of the cervical spine

needs re-evaluation and patients should be informed

about the possibility of a dissection and give con-

sent’ (75).

Disclosures

None.

E. ErnstComplementary Medicine,Peninsula Medical School,

Universities of Exeter & Plymouth,25 Victoria Park Road, Exeter EX2 4NT, UK

Email: [email protected]

References1 Ernst E. Adverse effects of spinal manipulation: a systematic

review. J R Soc Med 2007; 100: 330–8.

2 Leon-Sanchez A, Cuetter A, Ferrer G. Cervical spine manipulation:

an alternative medical procedure with potentially fatal complica-

tions. South Med J 2007; 100: 201–3.

3 Assendelft WJJ, Bouter LM, Knipschild PG. Complications of

spinal manipulation. A comprehensive review of the literature.

J Fam Pract 1996; 42: 475–80.

4 Stevinson C, Honan W, Cooke B, Ernst E. Neurological complica-

tions of cervical spine manipulation. J Roy Soc Med 2001; 94: 107–10.

5 Schievink WI, Mokri B, O’Fallon WM. Recurrent spontaneous

cervical-artery dissection. N Engl J Med 1994; 330: 393–7.

6 Rome PL. Perspective: an overview of comparative considerations

of cerebrovascular accidents. Chiro J Aust 1999; 29: 87–102.

7 Dixon P. Letter to the Editor. Adverse effects of spinal manipula-

tion. J R Soc Med 2007; 100(10): 444.

8 Lewis BJ. Letter to the Editor. Adverse effects of spinal manipula-

tion. J R Soc Med 2007; 100(10): 444.

9 Hill AB. The environment and disease: association or causation.

Proc Royal Soc Med 1965; 58: 294–300.

10 Terrett AGJ. Did the SMT practitioner cause the arterial injury?

Chiro J Aust 2002; 32: 99–110.

11 Lee VH. Incidence and outcome of cervical artery dissection: a

population-based study. Neurology 2006; 67: 1809–12.

12 Jones J. Neurologists warn about link between chiropractic,

stroke. CMAJ 2002; 166: 794.

13 Wright GT. Assessing the risks of cervical manipulation for neck

pain. CMAJ 2002; 166: 1134.

14 Haldeman S, Carey P, Townsend M, Papadopoulos C. Arterial

dissections following cervical manipulation: the chiropractic expe-

rience. CMAJ 2001; 165: 905–6.

15 Izquierdo-Casas J, Soler-Singla L, Vivas-Dıaz E, Balaguer-Martınez

E, Sola-Martınez T, Guimaraens-Martınez L. Diseccion vertebral

como causa del sındrome de enclaustramiento y opciones tera-

peuticas con fibrinolisis intraarterial durante la fase aguda. Rev

Neurol 2004; 38: 1139–41.

16 Kier AL, McCarthy PW. Cerebrovascular accident without chiro-

practic manipulation: a case report. J Manipulative Physiol Ther

2006; 29: 330–5.

17 Cassidy JD, Boyle E, Cote P et al. Risk of vertebrobasilar stroke

and chiropractic care: results of a population-based case–control

and case-crossover study. Spine 2008; 33(4S): S176–83.

18 Ernst E. Vascular accidents after chiropractic spinal manipulation.

Myth or reality? Perfusion 2009 (in press).

19 Smith WS, Johnston SC, Skalabrin EJ et al. Spinal manipulative

therapy is an independent risk factor for vertebral artery dissec-

tion. Neurology 2003; 60: 1424–8.

20 Hufnagel A, Hammers A, Schonle PW, Bohm KD, Leonhardt G.

Stroke following chiropractic manipulation of the cervical spine.

J Neurol 1999; 246: 683–8.

21 Donzis PB, Factor JS. Visual field loss resulting from cervical

chiropractic manipulation. Am J Opthalmol 1997; 123: 851–2.

22 Jones MR, Waggoner R, Hoyt WF. Cerebral polyopia with extras-

triate quadrantanopia: report of a case with magnetic resonance

documentation of V2 ⁄ V3 cortical infarction. J Neuroophthalmol

1999; 19: 1–6.

23 Hillier CEM, Gross MLP. Sudden onset vomiting and vertigo fol-

lowing chiropractic neck manipulation. J Postgrad Med 1998; 74:

567–8.

24 Garner LP, Case WF. Chiropractic manipulation and atheroscle-

rotic emboli to the eye. Am Fam Physician 1996; 53: 88–91.

25 Chung OM. MRI confirmed cervical cord injury caused by spinal

manipulation in a Chinese patient. Spinal Cord 2002; 40: 196–9.

26 Vibert D, Rohr-Le Floch J, Gauthier G. Vertigo as manifestation

of vertebral artery dissection after chiropractic neck manipula-

tions. ORL J Otorhinolaryngol Relat Spec 1993; 55: 140–2.

27 Yokota J, Amakusa Y, Tomita Y, Takahashi S. The medial medul-

lary infarction (Dejerine syndrome) following chiropractic neck

manipulation [in Japanese]. No To Shinkei 2003; 55: 121–5.

28 Brandt T, Orberk E, Weber R et al. Pathogenesis of cervical artery

dissections: association with connective tissue abnormalities.

Neurology 2001; 57: 24–30.

29 Haldeman S, Kohlbeck FJ, McGregor M. Unpredictability of cere-

brovascular ischemia associated with cervical spine manipulation.

Spine 2002; 27: 49–55.

30 Gouveia LO, Castanho P, Ferreira JJ, Guedes MM, Falcao F, e

Melo TP. Chiropractic manipulation: reasons for concern? Clin

Neurol Neurosurg 2007; 109: 922–5.

31 Rothwell DM, Bondy SJ, Williams JI. Chiropractic manipulation

and stroke: a population-based case–control study. Stroke 2001;

32: 1054–60.

32 Lipper MH, Goldstein JH, Do HM. Brown-Sequard syndrome of

the cervical spinal cord after chiropractic manipulation. Am

J Neuroradiol 1998; 19: 1349–52.

33 Tseng SH, Lin SM, Wang CH. Cervical epidural hematoma after

spinal manipulation therapy: case report. J Trauma Inj Infect Crit

Care 2002; 52: 585–6.

676 Perspective

ª 2010 Blackwell Publishing Ltd Int J Clin Pract, May 2010, 64, 6, 673–677

Page 5: Vascular accidents after neck manipulation: cause or coincidence?

34 Segal DH, Lidov MW, Camins MB. Cervical epidural hematoma

after chiropractic manipulation in healthy young women: case

report. Neurosurgery 1996; 39: 1043–5.

35 Tolge C, Iyer V, McConnell J. Phrenic nerve paby accompanying

chiropractic manipulation of the neck. South Med J 1993; 86:

688–90.

36 Schram DJ, Vosik W. Diaphragmatic paralysis following cervical

chiropractic manipulation: case report and review. Comple-

ment ⁄ Altern Med Asthma 2001; 119: 638–40.

37 Padua L, Padua R, LoMonaco M, Tonali PA. Radiculomedullary

complications of cervical spinal manipulation. Spinal Cord 1996;

34: 488–92.

38 Schmitz A, Lutterbey G, von Engelhardt L, von Falkenhausen M,

Stoffel M. Pathological cervical fracture after spinal manipulation in

a pregnant patient. J Manipulative Physiol Ther 2005; 28: 633–6.

39 Chen HC, Hsu PW, Lin CY, Tzaan WC. Symptomatic hematoma of

cervical ligamentum flavum: case report. Spine 2005; 30: E489–91.

40 Tome F, Barriga A, Espejo L. Multiple disc herniation after chiro-

practic manipulation [in Spanish]. Rev Med Univ Navarra 2004;

48: 39–41.

41 Tseng SH, Lin SM, Chen Y, Wang CH. Ruptured cervical disc

after spinal manipulation therapy: report of two cases. Spine 2002;

27: E80–2.

42 Oppenheim JS, Spitzer DE, Segal DH. Nonvascular complications

following spinal manipulation. Spine J 2005; 5: 660–7.

43 Nadgir RN, Loevner LA, Ahmed T et al. Simultaneous bilateral

internal carotid and vertebral artery dissection following chiro-

practic manipulation: case report and review of the literature.

Neuroradiology 2003; 45: 311–4.

44 Dziewas R, Konrad C, Drager B et al. Cervical artery dissection –

clinical features, risk factors, therapy and outcome in 126 patients.

J Neurol 2003; 250: 1179–84.

45 Rajendran D, Mullinger B, Fossum C, Collins P, Froud R.

Monitoring self-reported adverse events: a prospective, pilot

study in a UK osteopathic teaching clinic. Int J Osteopath Med

2009; 12: 49–55.

46 Rubinstein SM, Peerdeman SM, van Tulder MW, Riphagen I,

Haldeman S. A systematic review of the risk factors for cervical

artery dissection. Stroke 2005; 36: 1575–80.

47 Cagnie B, Jacobs F, Barbaix E, Vinck E, Dierckx R, Cambier D.

Changes in cerebellar blood flow after manipulation of the cervi-

cal spine using Technetium 99 methyl cysteinate dimer. J Manipu-

lative Physiol Ther 2005; 28: 103–7.

48 Terrett AGJ. Vertebrobasilar Stroke Following Manipulation. Des

Moines: National Chiropractic Mutual Insurance Company, 1996.

49 Argenson C, Francke JP, Sylla S, Dintimille H, Papasian S, di

Marino V. The vertebral arteries (segments V1 and V2). Anat Clin

1980; 2: 29–41.

50 Norris JW, Beletsky V, Nadareishvili ZG. Sudden neck movement

and cervical artery dissection. CMAJ 2000; 163: 38–40.

51 Sherman DG, Hart RG, Easton JD. Abrupt change in head posi-

tion and cerebral infarction. Stroke 1981; 12: 2–6.

52 Haynes M, Milne N. Color duplex sonographic findings in human

vertebral arteries during cervical rotation. J Clin Ultrasound 2001;

29: 14–24.

53 Dumas JL, Salama J, Dreyfus P, Thoreux P, Goldlust D, Chevrel

JP. Magnetic resonance angiographic analysis of atlanto-axial rota-

tion: anatomic bases of compression of the vertebral arteries. Surg

Radiol Anat 1996; 18: 303–13.

54 Weintraub MI, Khoury A. Critical neck position as an indepen-

dent risk factor for posterior circulation stroke. A magnetic reso-

nance angiographic analysis. J Neuroimaging 1995; 5: 16–22.

55 Selecki BR. The effects of rotation of the atlas on the axis: experi-

mental work. Med J Aust 1969; 1: 1012–5.

56 Schmitt HP, Betz H. Spasm of vertebral artery due to blunt

mechanical impact: phenomenon and problem. In: Voth D, Glees

P, eds. Cerebral Vascular Spasm. Berlin: de Gruyter, 1985: 241–9.

57 Gotlib AC, Thiel H. A selected annotated bibliography of the core

biomedical literature pertaining to stroke, cervical spine, manipu-

lation and head ⁄ neck movement. J Can Chiropr Assoc 1985; 29:

80–9.

58 Ladermann JP. Accidents of spinal manipulation. Ann Swiss Chi-

ropr Ass 1981; 7: 161–208.

59 Schmitt HP. Zur Inzidenz, Phatomorphologie und Pathomechanik

der Komplikationen bei der Manualtherapie der Halswirbelsaule.

In: Odenbach E, Lauterbach H, Verheggen-Buschhaus H, eds.

Fortschritt und Fortbildung in der Medizin. Jahrbuch 1983 ⁄ 84 der

Bundesaerztekamme. Koln: Deutscher Aerzteverlag, 1983: 461–71.

60 Schmitt HP, Tamaska L. Dissecting rupture of vertebral artery

with fatal thrombosis of vertebral and basilar arteries (author’s

transl) [in German]. Z Rechtsmed 1973; 73: 301–8.

61 Sherman MR, Smialek JE, Zane WE. Pathogenesis of vertebral

artery occlusion following cervical spine manipulation. Arch

Pathol Lab Med 1987; 111: 851–3.

62 Jentzen JM, Amatuzio J, Peterson GF. Complications of cervical

manipulation: a case report of fatal brainstem infarct with review

of the mechanisms and predisposing factors. J Forensic Sci 1987;

32: 1089–94.

63 Lyness SS, Wagman AD. Neurological deficit following cervical

manipulation. Surg Neurol 1974; 2: 121–4.

64 Cagnie B, Barbaix E, Vinck E, D’Herde K, Cambier D. Extrinsic

risk factors for compromised blood flow in the vertebral artery:

anatomical observations of the transverse foramina from C3 to

C7. Surg Radiol Anat 2005; 27: 312–6.

65 Symons BP, Leonard T, Herzog W. Internal forces sustained by

the vertebral artery during spinal manipulative therapy. J Manipu-

lative Physiol Ther 2002; 25: 504–10.

66 Ernst E. Manipulation of the cervical spine: a systematic review of

case reports of serious adverse events, 1995–2001. MJA 2002; 176:

376–80.

67 Ernst E. Ophthalmological adverse effects of (chiropractic) upper

spinal manipulation: evidence from recent case reports. Acta Oph-

thalmol Scand 2005; 83: 581–5.

68 Haldeman S, Kohlbeck FJ, McGregor M. Stroke, cerebral artery

dissection, and cervical spine manipulation therapy. J Neurol

2002; 249: 1098–104.

69 Ernst E. Cerebrovascular complications associated with spinal

manipulation. Phys Ther Rev 2004; 9: 5–15.

70 Di Fabio RP. Manipulation of the cervical spine: risks and bene-

fits. Physical Ther 1999; 79: 50–65.

71 Hardesty WH, Whitacre WB, Toole JF, Randall P, Royster HP.

Studies on vertebral artery blood flow in man. Surg Gynecol Obstet

1963; 116: 662–4.

72 Kojima N, Tamaki N, Fujita K, Matsumoto S. Vertebral artery

occlusion at the narrowed ‘scalenovertebral angle’: mechanical

vertebral occlusion in the distal first portion. Neurosurgery 1985;

16: 672–4.

73 Ernst E. Chiropractic: a critical evaluation. J Pain Symptom Man-

age 2008; 35: 544–62.

74 Auquier L. Les complications neurovasculaires des manipulations

du rachis cervical. Point de vue d’un expert judiciaire. Rev Med

Orthop 1998; 52: 14–5.

75 Hamann G, Felber S, Haass A et al. Cervicocephalic artery dissec-

tion due to chiropractic manipulations. Lancet 1993; 341: 764–5.

Perspective 677

ª 2010 Blackwell Publishing Ltd Int J Clin Pract, May 2010, 64, 6, 673–677