Cervical Spine Pre-Screening For Arterial Dysfunction

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ARTICLE IN PRESS

Manual Therapy 13 (2008) 278–288


www.elsevier.com/locate/math

Review

Cervical arterial dysfunction and manual therapy: A critical literature


review to inform professional practice
Roger Kerrya,, Alan J. Taylorb, Jeanette Mitchellc,d,e, Chris McCarthyf
a
Division of Physiotherapy Education, University of Nottingham, UK
b
Nottingham Nuffield Hospital, Nottingham, UK
c
Department of Zoology & Physiology, School of Biological Sciences, University of Wyoming, Laramie, USA
d
Department of Kinesiology & Health, Division of Health Sciences, University of Wyoming, Laramie, USA
e
Department of Physiotherapy, School of Allied Health Professions, University of the West of England, Bristol, UK
f
Warwick Emergency Care and Rehabilitation, The University of Warwick, UK
Received 28 September 2006; received in revised form 29 October 2007; accepted 30 October 2007

Abstract

An abundance of literature has attempted to provide insight into the association between cervical spine manual therapy and
cervical artery dysfunction leading to cerebral ischaemic events. Additionally, specific guidelines have been developed to assist
manual therapists in clinical decision-making. Despite this, there remains a lack of agreement within the profession on many issues.
This paper presents a critical, re-examination of relevant literature with the aim of providing a contemporary, evidence-informed
review of key areas regarding the neurovascular risks of cervical spine manual therapy.
From a consideration of case reviews and surveys, haemodynamic principles, and blood flow studies, the authors suggest that: (1)
it is currently impossible to meaningfully estimate the size of the risk of post-treatment complications; (2) existing testing procedures
have limited clinical utility; and (3) a consideration of the association between pre-existing vascular risk factors, combined with a
system based approach to cervical arterial haemodynamics (inclusive of the carotid system), may assist manual therapists in
identifying at-risk patients.
r 2008 Elsevier Ltd. All rights reserved.

Keywords: Manual therapy; Vertebrobasilar insufficiency; Internal carotid artery dissection; Cervical arterial dysfunction; Atherosclerosis

1. Introduction provide clinical guidance for the safest implementation


of such techniques and for pre-manipulative screening
Manual therapists are aware that cervical spine for vertebrobasilar insufficiency (VBI) (Barker et al.,
manual therapy (MT) techniques, particularly those 2001; Magarey et al., 2004; APA, 2006). However, there
involving full-range, high-velocity, rotational move- is still widespread uncertainty and controversy regarding
ments, hold inherent risks of insult to the vertebral the association between cervical spine MT and cervical
arteries (VAs) and internal carotid arteries (ICAs), arterial dysfunction (CAD), the reliability and validity
which can result in cerebral ischaemia, stroke, or death. of functional screening tests, the specificity and sensi-
Extensive reviews of contemporary evidence, and tivity of these tests in identifying at-risk patients, and the
reasoned debate, have been undertaken in an effort to medico-legal position of therapists and patients (Aus-
tralian Journal of Physiotherapy (AJP), 2001; Jull et al.,
Corresponding author. Division of Physiotherapy Education, 2002; Kerry, 2002; Refshauge et al., 2002; Brew, 2004;
University of Nottingham, Hucknall Road, Nottingham, NG5 1PB, Kerry, 2004).
UK Tel.: +44 (0) 115 8231790. The purpose of this paper is to present a summarised,
E-mail address: roger.kerry@nottingham.ac.uk (R. Kerry). critical re-examination of current available published

1356-689X/$ - see front matter r 2008 Elsevier Ltd. All rights reserved.
doi:10.1016/j.math.2007.10.006
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R. Kerry et al. / Manual Therapy 13 (2008) 278–288 279

literature concerning cerebrovascular accidents (CVAs) Rivett and Milburn, 1996), and a probable flaw with
in the context of MT. The review is non-systematic and retrospective studies is the questionable reliability of
aims to provide a broad picture of evidence and recall of past events. Therefore inferences regarding size
contemporary thought with regards to risks of cervical of risk should be made with caution.
spine management. Most prospective surveys do not calculate estimates of
risk incidence, some stating explicitly that it would be
1.1. Data sources and method impossible and misleading to do so (Stevinson, et al.,
2001). Prospective studies are also likely to report a
Literature searches were conducted for the years higher number of cases of post-MT vascular complica-
1990–2007, using the data-bases Medline (PubMed); tions, for example, (Leboeuf-Yde et al., 1997; Nadar-
CINAHL; Embase; AMED; CISCOM; and the Co- eishvili and Norris, 1999; Stevinson et al., 2001;
chrane Library. Search terms were ‘vertebral artery’, Magarey et al., 2004), than retrospective estimates
‘basilar artery’, ‘vertebrobasilar artery’, ‘internal carotid (because of under-reporting, reporting restrictions,
artery’; ‘anatomy and histology’, ‘cytology’, ‘embryol- non-association of event to treatment, etc) (Stevinson
ogy’, ‘injuries’, ‘innervation’, ‘pathology’, ‘physiology’, et al., 2001; Dupeyron et al., 2003). Dupeyron et al.
‘radiology’, ‘radionuclide imaging’, ‘ultrasonography’, (2003) suggest that post-MT VBI could be 30 times
‘ultrastructure’, and ‘adverse effects’, ‘adverse events’, higher than published. A recent prospective study on—
‘chiropractic’, ‘complications’, ‘manual therapy’, ‘osteo- chiropractors reported no incidents of serious adverse
pathy’, ‘physiotherapy’, ‘risk’, ‘safety’, ‘spinal manip- events (Thiel et al., 2007). Although a well-structured,
ulation’, ‘strokes’, ‘vascular accidents’. Related links, rigorous survey, it must be considered that, as stated
reference lists, personal files, www search engines and above, any study targeted at manual therapists is likely
some publications prior to 1990, considered relevant to provide unreliable data due to reporting bias and lack
according to the key terms used, were also searched. of awareness of what constitutes an adverse event.
This search strategy was designed to widen the search
beyond the confines of MT literature. 2.2. Narrative reviews
The search process resulted in 833 articles, of which
224 were considered relevant to MT (referring to These ranged from discursive (Rivett, 1995) to
manipulative and non-manipulative techniques) via the structured reviews (Haldeman et al., 1999), encompass-
themes selected for the discussion. Key clinical and ing several themes. Firstly, in considering estimates of
theoretical themes consistent within this literature base incidence, a major confounding variable is that the
are supported by a representation of the search results in actual incidence is unknown (Rivett, 1995; Assendelft et
this paper. The discussion and conclusions of this review al., 1996; Ernst, 2001a, b, 2004), partly because the
focus on the risk of cervical spine MT, the usefulness of number of persons in the population receiving MT is
screening tests in assessing at-risk patients, haemody- unknown or unreported. This apparent under-reporting
namic factors, and the nature and signs and symptoms (Assendelft et al., 1996; Ernst, 2004) may be influenced
of arterial changes and insufficiency. by MT practitioners’ awareness of post-treatment
CVAs, physicians not making the link between MT
and CVAs, or a low probability of cases being published
2. Reviews and surveys (Ernst 2001a, 2002).
As another theme illustrating potential vascular post-
Reviews and surveys attempt to establish risk factors MT trauma, Hurwitz et al. (1996) reviewed 145 reports
for, and incidence of, CVAs related to MT. of post-MT complications: of 118 documented cases, 21
patients died and 52 were left with serious neurological
2.1. Questionnaire surveys deficits. Ernst (2004) reported that between 1995 and
2003 in Britain, 300 patients were adversely affected by
Retrospective and prospective surveys reviewed in- cervical spine MT, the most frequently reported
clude reports by both manual therapists and non- complication being stroke following arterial dissection.
manual therapists (neurosurgeons, neurologists, vascu- These reports highlight the necessity of manual thera-
lar surgeons). Non-manual therapists’ surveys report a pists to be aware of mechanisms and presentations of
higher number of patients suffering post-MT complica- vascular trauma, and possible underlying pathology.
tions or associated symptoms (Dvorak et al., 1993; Lee Lastly, the validity of movement-based pre-MT
et al., 1995; Rivett and Milburn, 1997). screening tests is questioned (Kunasmaa and Thiel,
Retrospective surveys report estimates of CVA-risk 1994; Rivett, 1997), some authors suggesting that testing
incidence ranging from one in 9122 (Michaeli, 1993) to should be stopped (Thiel and Rix, 2005). Recent reports
five in one million (Haynes, 1994). Some estimates have have undertaken probability analysis to calculate the
been based on inadequate sample sizes (Haynes, 1994; sensitivity and specificity of functional tests, using data
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280 R. Kerry et al. / Manual Therapy 13 (2008) 278–288

(flow rates and reproduced symptoms) from blood flow weighed the risks. Frisoni and Anzola (1991) concluded
studies. Current reports present sensitivity of 0%–21% from 39 cases that a priori risk identification cannot be
and specificity of 23%–90% (Kerry and Rushton, 2003; made in the majority of cases; symptoms may develop
Gross et al., 2005; Ritcher and Reinking, 2005). some time after uneventful treatment; mortality/long-
term impairment occurs in 28% of cases, and a history
2.3. Systematic reviews of previous, transient neurological symptoms or upper
cervical spine laxity should contra-indicate any neck
Three major systematic reviews were identified (Ernst, movement-based treatment.
2001b, 2002; Rubinstein et al., 2005). Ernst (2001b) Haldeman et al. (2002a) looked specifically at the
investigated the safety of cervical spine MT by effect of referral bias on clinical perceptions of VA
summarising data of all prospective investigations. dissection risk. Based on analyses of data from an
From five prospective studies, it was concluded that insurance provider and a chiropractic survey, they
half of all patients experienced mild, transient adverse reported that 1 in 48 manual therapists were likely to
events following manipulation, that no reliable data of be aware of post-MT CVA, compared to 1 in 2
the incidence of adverse events exist, and that there is a neurologists. This discrepancy could explain the appar-
need for further prospective investigations. ent differences in perception and experiences between
In a systematic review of all original case reports these two professions.
between 1995 and 2001, Ernst (2002) retrieved 42 Rothwell et al. (2001) conducted a population-based
individual case reports of complications post-manipula- nested case-control review to test the association
tion, 18 of which reported arterial dissection causing between MT and CVAs. Of 582 cases reviewed, they
stroke. Again, it was concluded that, although serious suggested that vertebrobasilar accidents were five times
complications do occur, it is impossible to rate their more likely to occur if a patient had MT one week prior
incidence based on existing reported data, and large to the stroke, and VA-stroke cases were five times more
rigorous prospective trials are needed. likely to have received MT than the control group. This
Rubinstein et al. (2005) undertook a systematic review concurs with the report of Smith et al. (2003)
literature review, between 1966 and 2005, focussing on who, after comparing 151 arterial dissection cases with a
risk factors for VA or carotid artery (CA) dissection. control group, concluded that arterial dissection was five
Thirty-one case-control studies (from 1023 abstracts) times more likely to occur if MT had been administered
were assessed for their methodological quality. After within 30 days prior to, and twice as likely to have had
controlling for selection bias, lack of controls for increased neck/head pain preceding the stroke. They
confounding variables, and inadequate data analysis, concluded that VA dissection was independently asso-
there were still strong associations between VA or CA ciated with stroke and increased neck/head pain.
dissection and aortic root diameter (434 mm), mi- Haldeman et al. (2002a) reported that 92% of VA cases
graine, relative common CA diameter change during the presented with neck/head pain, and 25% reported a
cardiac cycle, and trivial trauma (ie associated with sudden onset of pain (suggestive of a dissection in
cervical spine MT), and weak associations were found progress). Haldeman et al. (2002b) concluded that they
for plasma homocysteine and recent infections. The two were unable to identify risk factors from the 64 medico-
MT papers (Rothwell et al., 2001; Smith et al., 2003) legal cases and propose that vertebrobasilar dissection
that Rubinstein et al. (2005) reviewed reported that few be considered an unpredictable, inherent, idiosyncratic,
cases supported a clear temporal association between and rare complication of MT.
treatment and arterial dissection (n ¼ 4). However, These surveys and reviews show that there is a need
Rubinstein et al. (2005) used a 24-h post-treatment for well-structured, large scale prospective surveys and
cut-off point, thereby missing potential latent cases (a trials to be undertaken (Rivett, 1995; Hurwitz et al.,
phenomenon previously reported by other authors). 1996; Shekelle and Coulter, 1997; Ernst, 2001b, 2004)
This calls into question the parameters set by these before a more realistic impression of the neurovascular
authors. risk of MT can be established (Dvorak et al., 1993;
Haynes, 1994; Senstad et al., 1996; Rivett and Milburn,
2.4. Case reviews 1997; Stevinson et al., 2001).

Terrett (1987) reported on 107 cases of post-MT


vascular accidents, between 1934 and 1986, equally 3. Haemodynamics, arterial trauma and vascular
distributed across the genders, with average ages of pathology
39.8 yrs (female) and 36.2 yrs (male). DiFabio (1999)
reported that death occurred in 18% of 177 cases and MT has been burdened by its ongoing focus on the
concluded that the literature at that time did not vertebral artery in isolation. Haemodynamic theory is a
demonstrate that benefits of cervical spine MT out- relatively new but important area of thinking in MT
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R. Kerry et al. / Manual Therapy 13 (2008) 278–288 281

(Taylor, 2001). It is well documented and understood, 1998), strangulation (Clarot et al., 2005), effort (run-
that blood flow in the VA and ICA systems is intricately ning) (Shimada et al., 2005), horse-hoof impact (Fletch-
linked via the circle of Willis (Cardon et al., 1998). It er et al., 1995), sneezing (Taylor and Kerry, 2005). These
follows, therefore, that both VA and ICA blood flow examples, although unremarkable in isolation, should
and pathology should be considered in pre-treatment alert clinicians to the possibility that traumatic vascular
risk assessment. injury may occur in the ICAs as well as the VAs.
ICA blood flow velocity and volume are significantly Furthermore, these arterial pathologies (VA and ICA)
greater than in the VAs (Paivansalo et al., 1998; are known to present as neuromusculoskeletal symp-
Schoning and Hartig, 1998; Sidhu, 2000; Scheel et al., toms, often isolated neck and head pain, without the
2000a, b). Therefore, the ICAs may have a significant commonly described VBI symptoms (Munari et al.,
compensatory role during cervical spine movement and 1994; Taylor and Kerry, 2005, Arnold et al., 2006). This
positioning. A negative pre-manipulative test relies concurs with other reports of VA dissection presenting
critically on the patency of the ICAs and unaffected as isolated neck pain (Krespi et al., 2002) and/or
VAs (see blood flow studies section) for adequate headache (Gates et al., 1997), without classical VBI
perfusion and, as such, tests the system as opposed to signs.
the concept that this somehow tests the VA in isolation. Although the literature suggests that the pathogenesis
This concept is illustrated by Weintraub and Khoury of arterial dissection remains uncertain, proposed risk
(1998), who examined ICA and VA blood flow changes factors include high plasma homocysteine concentra-
in patients with known underlying pathology. They tions (Giroud et al., 1994; Pezzini et al., 2002); specific
reported an absence of overt VBI symptoms on genotypes (Pezzini et al., 2002); hereditary connective
sustained end-range extension for 3–4 min in 160 cases tissue disorders (i.e. Ehlers – Danlos syndrome)
(mean age: 66 years), 25% of whom had VA hypoplasia (Schwarze et al., 2000); connective tissue disorders
associated with marked basilar artery flow alteration, (Brandt et al., 2001); fibromuscular dysplasia (Van
whilst unsuspected ICA occlusion occurred in six cases Damme et al., 1999), and recent infections (Grau and
and VA occlusion in two. Welch et al. (2000) also Buggle, 1999). There is much debate in the current
studied the effect of occlusion of the ICAs and VAs on literature as to the relevance and relative weight of these
the opposing vessel flow, and reported that flow in one proposed risk factors and, in particular, why some
part of the system was significantly influenced by individuals seem more prone to vascular injury and
occlusion in the other part. These studies draw attention pathology than others (Rubinstein et al., 2005).
to the need to be aware of the effects cervical spine As stroke or death is the ultimate adverse outcome of
positioning and to identify pre-existing vascular disease cervical spine MT (DiFabio, 1999), it is of note that ICA
as a reason for caution in both pre-treatment testing and dissection is reported to be the cause of stroke in up to
practice of MT. 20% of patients aged 18–44 years (Lisovoski and
Trauma to cervical blood vessels is generally classified Rousseaux, 1991). Across all age groups, stroke is
as either dissection resulting from direct trauma to the considered to be the leading cause of morbidity and the
vessel, or localised thrombogenesis and embolus forma- third-leading cause of mortality in the Western world
tion in response to endothelial damage (Caplan and (Flossmann et al., 2004). Li et al. (2005) reported that
Biousse, 2004). Either pathological state may lead to uncontrolled blood pressure is a key factor in the
stroke (Pollanen et al., 1992; Ross, 1999). Arterial aetiology of stroke. Although the actual pathophysiogi-
dissection may occur after trivial trauma to the vessel, or cal mechanisms of post-cervical spine MT stroke are
spontaneously. This may be related to pre-existing, largely unknown, the occurrence of VA and/or ICA
congenital weakness of the vessel wall or acquired dissection, with or without pre-existing vascular pathol-
vascular pathology (atherosclerosis). The mechanisms ogy, is the most commonly accepted theory. Manual
are thought to be arterial dissection with an intra-mural therapists should be acutely aware that patients may
haematoma, resulting in vessel lumen narrowing with present with headache and neck pain as the early
ensuing reduction in blood flow and ischaemia; an warning signs of impending stroke (Arnold et al., 2006).
extending dissection, leading to subarachnoid haemor- There are reports which suggest an association
rhage; and/or dissection leading to thrombus formation between ICA insufficiency/ischaemia and upper cervical
with secondary emboli, and stroke (Mann and Re- spine instability (Volle and Montazem, 2001; Tominaga
fshauge, 2001; Schievink et al., 2001). et al., 2002; Garg et al., 2004; Yamazaki et al., 2004).
ICA dissection has been linked to multiple types of There are also reports that demonstrate anterior and
non-penetrating or blunt trauma, including motor posterior blood flow dysfunction following road traffic
vehicle accidents (Miller et al., 2002; Beaudry and accidents (Chung and Han, 2002; Beaudry and Spence,
Spence, 2003), manipulation (Haneline et al., 2003; 2003). These two points are of relevance to MT and
Ernst, 2004), hand-held mechanical massagers (Grant should be given consideration, as pre-disposing factors,
and Wang, 2004), soft-ball injuries (Schievink et al., in the assessment of VA and ICA insufficiency.
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282 R. Kerry et al. / Manual Therapy 13 (2008) 278–288

Atherosclerosis is believed to be more prevalent in the contralateral cervical spine rotation (Tissington-Tatlow
ICAs than VAs in modern Western societies (Ersoy and Brammer, 1957; Toole and Tucker, 1960; Brown
et al., 2003; Giannoukas et al., 2005). However, VA and Tissington-Tatlow, 1963; Selecki, 1969). Later in
disease has been reported (Mitchell, 2002) and proposed vivo studies, using flowmetry, angiography, Doppler
as a risk factor for MT (Cagnie et al., 2006). VA and ultrasonography or magnetic resonance angiography,
ICA disease has been shown to co-exist in the same and documenting changes in VA blood flow before and
patients and may be accompanied by coronary and after cervical spine rotation, have produced contra-
peripheral occlusive disease and hypercholesterolaemia dictory results. Some researchers found no changes
(Caplan et al., 1992). A large body of literature in this (Weingart and Bischoff, 1992; Thiel et al., 1994; Haynes
area considers potential risk factors such as hyperten- and Milne, 2001; Zaina et al., 2003) while others
sion, smoking, diabetes, hypercholesterolaemia, hyper- reported a significant reduction in contralateral blood
homocysteineamia, factors affecting blood coagulation, flow (Refshauge, 1994; Rossitti and Volkmann, 1995;
vascular trauma, infection, and migraine (Ross, 1999; Licht et al., 1998a; Li et al., 1999; Rivett et al., 1998,
Pezzini et al., 2002; Westaway et al., 2003; Migdalski 1999; Mitchell, 2003; Arnold et al., 2004; Mitchell et al.,
et al., 2005; Arnold et al., 2006; Cagnie et al., 2006). This 2004).
emphasises the need to incorporate both localised and This controversy may be because there is no
systemic factors in pre-treatment clinical reasoning and standardisation of methods used. For example, healthy
risk assessment for all age groups. Contrary to this line subjects and patients, who may or may not have had
of thinking are the conclusions from a sole MT-specific signs and symptoms of VBI at the time of measurement,
study which found no association between such risk were used. Both young and older subjects were included
factors and reported cases of post-MT stroke (Halde- in some samples, and few authors compared males and
man et al., 2002c). This report of 64 cases over a 16 year females (Sturzenneger et al., 1994; Li et al., 1999; Rivett
period concluded that cerebrovascular accident follow- et al., 1999; Haynes et al., 2000; Scheel et al., 2000a, b;
ing manipulation was an unpredictable phenomenon. Mitchell, 2003, 2007).
However, pre-incident data (the most important when Blood flow measurements at pre-transverse, cervical
considering profiling for chance of adverse event) was and intracranial parts of the VA have been reported.
only available in 41% of the 64 cases reported, the range The cervical VA, as it traverses the bony transverse
of events was restricted (i.e. only those that occurred foramina, is difficult to insonate accurately which may
within 48 h of a manipulation treatment and those which have confounded the findings (Johnson et al., 2000;
happened to get to the attention of a single physician), Khaw et al., 2004). There is a logical argument that it is
and the range of atherosclerotic risk factors was narrow the change in blood flow in the intracranial part of the
and not representative of contemporary evidence-based VA (distal to the point of constriction) and not in the
risk factors. Considering these points, and the over- more proximal extracranial VA, that may correlate with
whelming amount of literature relating atherosclerosis potential hindbrain ischaemia most accurately (Zaina
to stroke, it is difficult to refute the hypothesis that post- et al., 2003; Mitchell, 2005, 2008). However, few studies
MT strokes are associated with vascular pathology. report blood flow measurements at this site (Rossitti and
It is clear that the interaction between mechanisms of Volkmann, 1995; Li et al., 1999; Mitchell, 2003; Mitchell
vascular injury, underlying hereditary disorders, and et al., 2004).
proposed risk factors adds a body of new information Various degrees of cervical spine rotation and
for consideration. This knowledge may direct both the extension have been implicated in compromised VA
clinical reasoning process and future research into pre- blood flow and associated VBI (Refshauge, 1994;
treatment cervical risk assessment. This may direct Sturzenneger et al., 1994; Licht et al., 1998b; Rivett
research toward the model used in suspected thrombo- et al., 1998, 1999; Li et al., 1999; Scheel et al., 2000a;
embolism (Fancher et al., 2004), a condition which Haynes and Milne, 2001). Reports of the effect of
mirrors VA and ICA dissection in its complex patho- cervical spine rotation on both ICA and VA blood flow
genesis and level of difficulty to diagnose or predict found either no significant change in ICA blood flow or
accurately. a decrease in both VA and ICA blood flow on rotation
and extension. (Schoning et al., 1994; Rivett et al., 1999;
Scheel et al., 2000a, b; Licht et al., 2002). An increase
4. Blood flow studies followed by a decrease in VA and ICA blood flow at 451
and full rotation, respectively, is also reported (Re-
The effects of cervical spine movements upon VA fshauge, 1994). Therefore, it is apparent from these
blood flow have long been reported, with little studies that blood flow changes in both the VA and
consideration of ICA blood flow and haemodynamic ICA, associated with cervical spine movements, should
compensatory principles. Initial cadaver experiments be taken into account in patient pre-treatment risk
showed decreased VA blood flow, particularly on assessment.
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R. Kerry et al. / Manual Therapy 13 (2008) 278–288 283

Some researchers, using patients experiencing mild rotation and observing the reproduction of cardinal
signs of VBI, found a decrease in blood flow (at mid- signs and symptoms). Many blood flow studies that
cervical levels) on cervical spine rotation (Rivett et al., demonstrate changes in blood flow during cervical spine
1999). Others found no significant decrease in VA blood rotation, for example, conclude that their findings
flow (at the pre-transverse level), despite positive VBI support the use of the functional test (the test uses the
signs reported by their subjects (Licht et al., 2000, 2002). position to alter blood flow, altered blood flow has been
It is not clear from these findings if the VBI symptoms demonstrated in this study, therefore the test is valid).
altered with cervical spine rotation. It is notable that However, there is little evidence to indicate a correlation
most of the studies of decreased blood flow following between blood flow changes and symptoms of VBI
rotation, using normal subjects aged 20–40 years, report (Licht et al., 1998a; Mitchell, 2003, 2007; Mitchell et al.,
no accompanying signs and symptoms of VBI. There- 2004). Thus, a subject can have reduced blood flow to
fore, it is apparent that no correlation between cervical the brain but display no signs of cerebral ischaemia. It
spine rotation and VBI symptoms can be clearly has been reported earlier that the ICA and VA arterial
established from this research. supplies are parts of an interdependent and compensa-
The contradictory findings of these studies preclude tory system. Therefore, it is unlikely that ischemic signs
definitive conclusions being made and emphasise the would be displayed if there is adequate compensatory/
need for more rigorous research into the complex collateral blood flow.
relationship between cervical spine movement and blood The disparity between symptoms and blood flow has
flow changes which must, at this stage, be regarded as a been highlighted further by probability analysis regard-
guide only in pre-treatment assessment. ing utility of the functional test, which has reported its
poor sensitivity and variable specificity (Kerry and
Rushton 2003; Gross et al., 2005; Ritcher and Reinking,
5. Discussion and conclusions 2005). At the current level of evidence, pre-manipulative
screening tests should be considered no more clinically
This review of contemporary literature regarding valuable than Homan’s test, for example, which is still
cervical spine MT and arterial insufficiency highlights used as a small part of wider examination procedures–in
several areas of clinical importance and many of the lower limb deep vein thrombosis risk assessment
outcomes correspond with previously published reviews protocols despite its known poor reliability (Levi
in this subject area. There are some findings, however, et al., 1999).
which add to existing MT knowledge and hence may The cardinal signs and symptoms of VBI also lack
influence the development of clinical reasoning and consistent support from the literature reviewed. There is
research. This review, therefore, serves to inform a diversity of presentations demonstrated in the cases
professional practice. reviewed. The most consistent recurring sign of VA and
Most blood flow studies reported refer to VA blood ICA dysfunction is an increase in neck/head pain.
flow in relation to cervical spine movement. Although Localised, somatic pain referral, related to the ICA
some studies report negative findings, there is an overall (Munari et al., 1994) and the VA (Krespi et al., 2002),
trend suggesting that both VA and ICA blood flow are has been reported. This presents an obvious diagnostic
influenced by full-range cervical spine movements, challenge for the manual therapist. Other symptoms can
although there are not always corresponding cerebro- be attributed to dysfunction of the ICA (e.g. Horner’s
ischaemic symptoms. There is evidence that cervical syndrome, flashing sensations) and may be erroneously
spine movement, principally rotation, influences VA interpreted as VBI, or of more concern, because these
blood flow. ICA blood flow has been shown to be symptoms do not form part of the classic cardinal signs,
influenced more by extension with rotation (Scheel et al., not attributed to a neurovascular cause at all.
2000a, b), with some other reports implicating extension An interesting trend in the literature is the distinction
as the most influential movement for ICA flow (Hane- between younger patients (o45 years) who have been
line et al., 2003). It is of interest to note here that the reported to suffer spontaneous or traumatic dissection
extension component of functional testing has been but may not demonstrate any of the classical vascular
removed from MT pre-treatment guidelines (Magarey risk factors (Rubinstein et al., 2005), and older patients
et al., 2004; APA, 2006). (445 years), who show signs of vascular pathology,
Recent guidelines (Magarey et al., 2004; APA, 2006) including atherosclerosis of the cervical vessels (Caplan
aim to assist in identifying patients who are more likely et al., 1992; Cagnie et al., 2006), who may demonstrate
to suffer adverse neurovascular events should a parti- classical (general or systemic) risk factors for vascular
cular treatment technique be used. One of the central disease. However, other reports have suggested that,
components to the guidelines for pre-treatment screen- based on a cadaver study, the presence of VA
ing of patients is the performance of a functional atherosclerosis in young (o45 years) subjects cannot
positioning test (the VBI test involving cervical spine be excluded (Mitchell, 2002). This illustrates the
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284 R. Kerry et al. / Manual Therapy 13 (2008) 278–288

importance of understanding the complexity of CAD, Bronfort et al., 2001; Hoving et al., 2002; Jull et al.,
particularly that cerebral ischaemia may occur due to a 2002a) with increasing evidence that cervical MT alone,
variety of underlying factors and pathologies. or as part of multi-modal management strategy, is
Considering that there is a risk, it is important to beneficial for the relief of neck pain (Hurwitz et al.,
consider the size of the risk. Many reviews attempt to 1996; Bronfort et al., 2004; Gross et al., 2004).
establish a risk ratio, but these are misleading figures In order to make a statistically driven decision on the
based on under-reporting, methodological flaws, and an risk:benefit ratio, valid data are needed on both sides of
erroneous perception of probability. The actual risk of this analysis. As stated earlier, valid data relating to size
post-treatment complications cannot be determined of risk is incomplete. Intervention choices must also be
from the available evidence, and neither clinicians nor made in the context of alternative interventions and
patients should be misled into believing that the risk is their known risks. Commonly, authors compare cervical
of a particular, established magnitude. The risk should MT with common medical interventions, such as non-
be calculated on all current factors surrounding the steroidal anti-inflammatories, and state that the risk of
particular situation at the particular time, for each MT is less than the known risks associated with
patient. medication (Dabbs and Lauretti, 1995; Hurwitz et al.,
There have been few reports explicitly categorising 1996; Jull et al., 2002). Although this is likely, without
definitive risk factors for VA and ICA dysfunction. supporting data such claims should be noted with a
Some have suggested that post-treatment accidents are degree of caution.
unpredictable and that there are no definitive risk Despite the lack of data, a small number of authors
factors (Haldeman et al., 2002b). There are too few have commented specifically on the risk:benefit judge-
reports, however, which have focussed specifically on ment and have come to firm conclusions. DiFabio
risk factors to make a conclusive judgment on this issue. (1999) explicitly states that the risks of cervical
Only well-structured, large prospective investigations manipulation outweigh the benefits. This follows a
could provide this information. There is a consistent review of 177 cases of adverse events in the context of
suggestion in the literature reviewed that compromised selected literature exploring the proposed benefits of
blood flow to the brain and thrombo-embolic events are cervical manipulation. Conversely, a more recent study
related to various established vascular disease risk states that the potential benefits of cervical therapy do
factors (hypertension, hypercholesterolaemia, athero- outweigh the risks (Rubinstein et al., 2007). This
sclerosis, trauma, infection, migraine etc). In the absence statement is based on the results of a prospective
of strong evidence against this link, it might be prudent follow-up survey of clinicians’ reports of responses to
for the manual therapist not to dismiss such risk factors. treatment (as discussed above). Similarly, whilst this is
Considering the inconsistencies in supporting evi- likely to be the case, such judgements need to be
dence for: (1) cardinal signs of arterial insufficiency; (2) considered in the context of the limitations of the data
validity of functional testing; and (3) identification of and methodologies.
definite risk factors (for post-manipulation vascular Childs et al. (2005) embrace the inherent uncertainties
injury), the acceptance of and adherence to clinical in this clinical area and provide discussion on making
guidelines that incorporate inclusion of these areas reasoned judgements in the absence of good data – not
presents an interesting professional challenge. The only for risks and benefits, but also in respect of the
present medico-legal climate makes unreasoned compli- validity of screening procedures for potential risk. The
ance to guidelines that are not based on consistent outcomes of this review reflect this thinking: incorpor-
evidence legally indefensible, and the opinions of expert ating knowledge of haemodynamic and vascular patho-
witnesses may be challenged in court (Bolitho v City and physiology into patient assessment may lead the
Hackney, 1997; Foster, 2002, p. 116). clinician to an informed judgement as to the likelihood
of serious adverse events. If the limitations of traditional
5.1. Risk versus benefit screening processes are understood and the evidence
regarding benefit considered, a sound and reasonable
This paper has purposefully focussed on potentially decision may be reached regarding choice of interven-
serious adverse cervico-cranial events associated with tion.
MT. It was not the intention of the authors to report
specifically on the suspected benefits of cervical MT. 5.2. Recommendations
However, in the clinical decision-making process, it is
unrealistic to consider risk without benefits, and vice There is a clear need for further research in a number
versa. of areas in this field. The indication for large-scale,
There have been several randomized controlled trials robust, prospective trials has been consistently reported
investigating the effectiveness of cervical MT (e.g. Koes as the best way to establish a reliable indicator of risk of
et al., 1992a, b; Boline et al., 1995; Nilson et al., 1996; arterial insufficiency related to cervical spine MT.
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However, considering the size of the task, this would be Arnold M, Cumurciuc R, Stapf C, Favrole P, Berthet K, Bousser MG.
logistically difficult. Until a stronger evidence-base can Pain as the only symptom of cervical artery dissection. Journal of
be established, it is advisable that manual therapists take Neurology Neurosurgery and Psychiatry 2006;77(9):1021–4.
Assendelft WJJ, Bouter LM, Knipschild PG. Complications of spinal
note of the available evidence supporting all of the manipulation—a comprehensive review of the literature. The
possible generic vascular risk factors, prior to cervical Journal of Family Practice 1996;42(5):475–80.
spine MT. Based on the findings of this review, the Australian Physiotherapy Association (APA). Clinical guidelines for
authors make the following recommendations: assessing vertebrobasilar insufficiency in the management of
cervical spine disorders. /www.Physiotherapy.asn.auS. 2006.
Australian Journal of Physiotherapy (AJP). Forum: pre-manipulative
1. Considering the limited support for the use of cervical
testing of the cervical spine. Australian Journal of Physiotherapy
spine functional pre-manipulative screening tests (e.g. 2001;47(3):163–8.
the VBI test), as an indicator of either vascular Barker S, Kesson M, Asmore J, Turner G, Conway J, Stevens D.
patency or of the propensity of blood vessels to be Guidance for pre-manipulative testing of the cervical spine.
injured as a result of MT, these tests should be used Physiotherapy 2001;87(6):318–22.
with caution and the results should be interpreted in Beaudry M, Spence JD. Motor vehicle accidents: the most common
cause of traumatic vertebrobasilar ischemia. Canadian Journal of
the knowledge that the tests have little backing from Neurological Sciences 2003;30(4):320–5.
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edge). connective tissue abnormalities. Neurology 2001;57(1):24–30.
3. Headache and neck pain are common presenting Brew J. Consent to touch, consent to treat. Invited address. CSP
signs of vascular dissection. Therefore, careful con- Congress 2004, Birmingham, UK.
sideration of the differential diagnosis of these Bronfort GR, Evans R, Nelson B, Aker PD, Goldsmith CH, Vernon
H. A randomized clinical trial for patients with chronic neck pain.
symptoms by the manual therapist is recommended. Spine 2001;26:788–99.
4. As cervical artery haemodynamics (inclusive of the Bronfort G, Haas M, Evans RL, Bouter LM. Efficacy of spinal
ICA and therefore the system) are influenced by manipulation and mobilisation for low back pain and neck pain: a
movement as a whole, and not exclusively by single systematic review and best evidence synthesis. The Spine Journal
thrust manipulative procedures, vascular risk assess- 2004;4:335–56.
Brown BStJ, Tissington-Tatlow WF. Radiographic studies of the
ment should be considered prior to all manual
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risk assessment to the VA in isolation may represent a 28(2):129–34.
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Acknowledgements
12(6):579–82.
Childs JD, Flynn TW, Fritz JM, Piva SR, Whitman JM, Wainner RS,
The authors would like to acknowledge the support of Greenman PE. Screening for vertebrobasilar insufficiency in
and thank: the Manipulation Association of Chartered patients with neck pain: manual therapy decision-making in the
Physiotherapists (MACP) for its support in this project; presence of uncertainty. Journal of Othopaedic and Sports
Steven Barrett and the Research Support Unit, Uni- Physiotherapy 2005;35(5):300–6.
Chung YS, Han DH. Vertebrobasilar dissection: a possible role of
versity of Nottingham, for assistance in the literature whiplash injury in its pathogenesis. Neurological Research
searches involved in this review; and Lindsay Skipper, 2002;24(2):129–38.
University of Nottingham for proof-reading this paper. Clarot F, Vaz E, Papin F, Proust B. Fatal and non-fatal bilateral
delayed carotid artery dissection after manual strangulation.
Forensic Science International 2005;149(2–3):143–50.
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