The effect of a simulated manipulation position on internal carotid and vertebral artery blood flow in healthy individuals

Manual Therapy 16 (2011) 87e93

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Original article

The effect of a simulated manipulation position on internal carotid and vertebral artery blood flow in healthy individuals Neil Bowler a, *, Delva Shamley b, Rachael Davies c a

School of Health & Social Care, Oxford Brookes University, Jack Straws Lane, Oxford OX3 0FL, UK Clinical Trials Development, Centre of Postgraduate Medical Research and Education, Bournemouth University, Royal London House, Christchurch Road, Bournemouth BH1 3LT, UK c Vascular Lab, Nuffield Department of Surgery, John Radcliffe Hospital, Headley Way, Oxford OX3 9JE, UK b

a r t i c l e i n f o

a b s t r a c t

Article history: Received 9 November 2009 Received in revised form 8 July 2010 Accepted 13 July 2010

The simulated manipulation position is one of several premanipulative screening tests recommended to assist in identifying patients at risk of complications from high velocity thrust manipulation of the cervical spine. The effects of this position on blood flow in the vertebral artery has been measured, but not in the internal carotid artery. Fourteen healthy subjects participated in a pre-test post-test single group study to determine the effect of a simulated manipulation position on blood flow in both the internal carotid and vertebral arteries. Duplex ultrasound with colour Doppler imaging was used to image the internal carotid and vertebral arteries and to measure blood flow velocity with the neck in neutral and simulated manipulation positions. A measure of distal vascular resistance, the resistance index, was calculated. There was a significant (p < 0.05) reduction in the resistance index in the vertebral arteries ipsilateral to the rotation component of the simulated manipulation position. Placing the cervical spine in a simulated manipulation position, did not adversely affect blood flow through the internal carotid and vertebral arteries. Further research is needed to determine how the simulated manipulation position affects internal carotid and vertebral artery blood flow in individuals who have signs or symptoms of neurovascular insufficiency. Ó 2010 Elsevier Ltd. All rights reserved.

Keywords: Manipulation Internal carotid artery Vertebrobasilar Blood flow

1. Introduction Neck pain, worldwide, has a 1-year prevalence estimated to range from 12.1% to 75.1% and a 1-month prevalence from 15.4% to 45.3% (Fejer et al., 2006; Hogg-Johnson et al., 2008). Prevalence is highest among women and peaks in middle age (Fejer et al., 2006; Hogg-Johnson et al., 2008). A pathoanatomical cause cannot be identified in the majority of patients complaining of neck pain and neck related symptoms of the upper quarter (Borghouts et al., 1998). However, once medical pathology such as cervical fracture, myelopathy or inflammatory arthropathies, have been excluded, patients are often classified as having either a nerve root compromise or a ‘mechanical neck disorder’ (Childs et al., 2008), both of which are treated by therapists. Therapy management of mechanical neck disorders includes manual therapy, therapeutic exercise, ergonomics and education. Manual therapy utilises passive joint movement techniques, and in this study the term

* Corresponding author. Tel.: þ44 1865 485268; fax: þ44 1865 482775. E-mail address: [email protected] (N. Bowler). 1356-689X/$ e see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.math.2010.07.007

‘manipulation’ will refer to such techniques performed as highvelocity, low-amplitude ‘thrusts’ (Maitland et al., 2005). There is considerable evidence in systematic reviews to support the use of manipulation techniques in the cervical spine for the treatment of neck pain and headache (Hurwitz et al., 1996; Vernon et al., 1999; Bronfort et al., 2004; Gross et al., 2004; Vernon et al., 2005; Vernon et al., 2007). Manipulation of the neck however, is associated with a risk of adverse neurovascular events such as transient ischaemic attack, stroke or death, most commonly due to arterial dissection of the vertebral artery (VA) or to a lesser extent of the internal carotid artery (ICA) (Frisoni & Anzola, 1991; Assendelft et al., 1996; Di Fabio, 1999; Stevinson & Ernst, 2002; Ernst, 2004, 2007). The risk of adverse neurovascular events due to cervical manipulation has been estimated by calculating the ratio of the incidents reported per estimated number of treatments. Such calculations vary from 3:7500 to 1:5 million (Haldeman et al., 2001; Ernst, 2004). However, such estimates may be inaccurate due to recall bias and under-reporting. Guidelines for pre-manipulative screening of patients at risk of arterial complications have been developed with particular emphasis on an assessment of vertebrobasilar insufficiency

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(Barker et al., 2000; Rivett et al., 2006). The latest guidelines (Rivett et al., 2006) include a pre-manipulative assessment for any symptoms of vertebrobasilar insufficiency which may be elicited by positioning the cervical spine in end-range rotation, extension, combined extension/rotation, and in the Simulated Manipulation Position (SMP). The SMP is a pre-manipulative hold of the cervical spine in a position in which the high velocity thrust is to be applied. Provocation of symptoms during or immediately after testing constitutes a positive test and would contraindicate cervical manipulation. The theoretical basis for the physical screening tests described is that the mechanical stresses imposed on the ICAs and VAs in the various test positions may reduce the diameter of the lumen of the vessels and thereby affect blood flow. It is suggested that provocation of ischaemic symptoms with positional testing indicates insufficient cerebral perfusion. The screening tests are therefore intended to assess the adequacy of blood supply to the brain during extreme movements and thereby identify those patients who may be at risk of serious neurovascular complications after cervical manipulation. Only one study was found which investigated the effect of a SMP on blood flow (Arnold et al., 2004). Peak systolic velocity (PSV) and end diastolic velocity (EDV) were measured at approximately C3-5 level in both VAs and a resistance index (RI) was calculated according to the formula RI ¼ (PSV  EDV)/PSV. High resistance in distal vessels due to stenosis produces low diastolic flow in the supplying artery and results in a high value for this index (Allan et al., 2006). Arnold et al. (2004) found a significant (p < 0.05) reduction in PSV and EDV, and a significant (p < 0.05) increase in the RI in the contralateral VA, indicative of narrowing of the artery distally. In the ipsilateral VA the PSV and EDV increased and the RI decreased, however, only the change in EDV was significant (p < 0.05). To the authors’ knowledge, no studies have investigated the effect of a SMP on blood flow in the ICAs. If a screening test such as the SMP is intended to assess the adequacy of overall blood supply to the brain, the extent and manner in which blood flow is affected in both the ICAs and VAs simultaneously is important. Prior to investigating the effect of the SMP on blood flow in subjects who are positive on premanipulative testing, it is valuable to establish normal data for such effects in asymptomatic individuals as this will allow for more accurate interpretation of subsequent clinical data (Licht et al., 1998; Licht et al., 1999). The aim of this study was to investigate if the SMP produces measurable and significant changes in ICA and VA blood flow compared to a neutral neck position in healthy adults. The study was approved by the National Health Service Research Ethics Committee.

with an information sheet and given the opportunity to discuss the study with the researcher. After obtaining informed written consent, potential subjects were screened by telephone interview using a standardised screening schedule. This covered details of their history, symptoms, or medications which would put them at risk of injury and would normally contraindicate cervical spine manipulation. Remaining subjects were then further screened by physical examination to exclude those with pain on active cervical movement and those with any signs or symptoms on sustained cervical spine rotation, combined extension/rotation, or the SMP. These positions were held for at least 10 s followed by at least 10 s in the neutral position to assess for any latent responses (Rivett et al., 2006). Both the interview and physical examination were conducted by the principal investigator, a physiotherapist with post-graduate musculoskeletal training and 26 years of clinical experience. 2.3. Simulated manipulation position (SMP) The SMP used in this study was for a C2/3 manipulation technique in which the head is rotated to one side until movement can first be palpated at C2/3. Side-flexion to the opposite side is then added, again until tension can be palpated at C2 (Fig. 1). This sequence of movements and position are used in preparation for two commonly used manipulation techniques e the ‘transverse thrust’ manipulation (Maitland et al., 2005) and the ‘up-slope gliding’ manipulation (Gibbons & Tehan, 2006). 2.4. Data collection: instruments and procedures Subjects attended the vascular laboratory at the John Radcliffe Hospital for data collection. The procedure commenced with subjects resting in supine lying for 5 min to allow for a period of haemodynamic stabilisation (Rivett et al., 1999; Arnold et al., 2004). A Philips iU22 ultrasound machine (Koninklijke Philips Electronics N.V., Eindhoven, Netherlands) with a broadband (9e3 MHz) linear array transducer was used to measure blood flow velocity in both left and right ICA and VA with the subject’s neck in a neutral position, supine lying without pillows. The neutral position was maintained by the principal investigator while the common carotid, ICA and VA were scanned and examined for pathology. Colour Doppler was used to identify the vessels and blood flow velocities were obtained using spectral Doppler from the ICA at 1e2 cm above the carotid bulb and from the VA at the same

2. Methods 2.1. Sample size It was calculated that the study would require at least 14 subjects. This was based on a significance level of 5%; a power of 80%; a standard deviation in blood flow velocity of 18 cm/s (Schoning et al., 1994; Scheel et al., 2000); and a mean percentage change in blood flow velocity of 26% (selected after consideration of Doppler variation (Grant et al., 2003), volume flow rate as a function of average velocity and area (Allan et al., 2006), and ultrasound machine variability (Hoskins, 1996)). 2.2. Recruitment and selection Advertising posters placed within Oxford Brookes University were used to recruit a convenience sample of subjects to the study. Individuals responding to the advertising posters were provided

Fig. 1. The simulated manipulation position.

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segmental level (i.e. approximately C2/3). The position of the probe on the skin was marked. The sample volume was set at about onethird of the total diameter and placed in the centre of the vessel in order to avoid the natural turbulence at the edge of the lumen (Allan et al., 2006). The Doppler angle was maintained at 56 in order to avoid overestimation of the velocity (Mohler et al., 2006). Three measures of peak systolic velocity (PSV) and of end diastolic velocity (EDV) were taken for each artery in the neutral position. The principal investigator then positioned the subject’s neck in the SMP on one side while ICA and VA blood flow velocity was remeasured with the probe in the same position on the skin. The SMP was held for at least 10 s before scanning commenced, and as long as necessary to obtain all measurements (Rivett et al., 2006). Again, three measures of PSV and of EDV were taken of each artery. Testing was discontinued on provocation of any signs or symptoms. The subject’s neck was then returned to a neutral position for a 60 s rest period while an assessment was made of any latent signs or symptoms. The whole procedure was then repeated with the neck in the neutral position and in the SMP on the opposite side. 2.5. Study reliability The side to commence the SMP was selected randomly for the first subject. Thereafter, the SMP was commenced on the alternate side for each subsequent subject. By counterbalancing in this way, any bias in the results due to order effects is balanced out (Hicks, 2004). The same vascular ultrasonographer with extensive experience in the examination of the ICAs and VAs performed all Doppler ultrasound scans. A practice session was undertaken prior to data collection in order to familiarise the ultrasonographer with the study protocol and to ensure that both VAs and ICAs could be located and sampled in the SMP. 2.6. Data analysis SPSS version 17.0 was used for statistical analysis. Three measures were taken of PSV and of EDV for each artery in each subject. The mean of these three values was calculated to reduce random errors (Gill, 1985). The mean PSV and EDV were then used to calculate a RI and overall mean blood flow velocity (VMean) according to the formula VMean ¼ [(PSV  EDV)/3] þ EDV (Mitchell, 2009). In order to determine whether the data was normally distributed, the KolmogoroveSmirnov and ShapiroeWilk tests were conducted. To determine any significant differences between blood flow parameters in the neutral position and SMP, the related two-tailed t-test was conducted on all normally distributed data, and the Wilcoxon signed-rank test was conducted on data which was not normally distributed. 3. Results Fourteen subjects with a mean age of 31 years (SD ¼ 10.76, range 19e49) were included in the study. There were 11 females (mean age 31 years) and 3 males (mean age 31 years). None of the subjects had signs of vascular pathology in the common carotid, ICA or VA on routine colour duplex scanning. The mean time held in the SMP was 4 min 52 s. No discomfort or signs and symptoms of arterial ischaemia were experienced by any of the subjects during data collection and as such all participant data is included in the analysis. An example of the Duplex ultrasound image and spectrograms for the ICA and VA are shown in Figs. 2 and 3 respectively.

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The ICA and VA can be seen in the combined colour Doppler/ B-mode images at the top of Figs. 2 and 3 respectively. Two cursor markers can be seen on the spectrograms at the bottom of each Figure. The top cursor is positioned to measure the PSV and the lower cursor is placed to measure the EDV. The key in the middle of each Figure shows the values of these velocities. Mean data from all participants was pooled, and a group mean is shown for the ICAs in Table 1, and for the VAs in Table 2. In the initial neutral position, there was significantly greater (p ¼ 0.008) EDV in the right ICA compared to the left ICA. There were no other significant differences in any of the blood flow parameters between left and right ICAs or VAs in the neutral position. There was a statistically significant increase (p ¼ 0.018) in the EDV of the left ICA from neutral to the SMP (LR/RSF). This increase in EDV was reflected in a statistically significant (p ¼ 0.002) decrease in the RI of the left ICA from neutral to the SMP (LR/RSF). The RI decreased significantly from neutral to the SMP (LR/RSF) in both the left VA (p ¼ 0.027) and right VA (p ¼ 0.043). The RI also decreased significantly from neutral to the SMP on the opposite side (RR/LSF) in the right VA (p ¼ 0.027). There were no statistically significant differences in any other blood flow parameters of any artery between neutral and either SMP. 4. Discussion The results of this study do not provide any evidence that blood flow through the ICAs and VAs in healthy individuals is adversely affected by placing the cervical spine in a SMP. The increased EDV in the left ICA was accompanied by a significant decrease in the RI in the left ICA in the same SMP (LR/RSF). This is in accordance with the formula RI ¼ (PSV  EDV)/PSV, and is based on the premise that EDV is likely to increase to a greater extent by lower resistance than PSV, resulting in a fall in the index. The significant reduction in distal resistance seen in the left ICA in the SMP (LR/RSF) was however, not seen in the right ICA in the SMP to the opposite side (RR/LSF). One consistent bilateral pattern within these findings was a decrease in the RI of the VA ipsilateral to the rotation component of the SMP i.e. decreased RI in the left VA in SMP (LR/RSF) and decreased RI in the right VA in SMP (RR/LSF)). Arnold et al. (2004) reported their results in the contra- and ipsi-lateral directions in relation to the VA. These terms were used in relation to the rotation component of the SMP (Arnold & Bourassa, Personal Communication). Hence, the findings of a decrease in the RI of the ipsilateral VA in the SMP support those of Arnold et al. (2004), although their results for this change were not statistically significant (p > 0.05). There was no support for the finding of a significant increase in the RI of the contralateral VA in the SMP by Arnold et al. (2004). In fact, in the current study, the mean RI in the right VA decreased significantly (p < 0.05) in the SMP (LR/RSF). Arnold et al. (2004) also found a pattern of increased PSV and EDV in the ipsilateral VA in the SMP, and decreased PSV and EDV in the contralateral VA in the SMP. No consistent pattern of change in these parameters for the VAs was found in the current study. Subject demographics were not substantially different between the current study and Arnold et al. (2004), who had 14 females and 8 males with a mean age of 35 years (SD ¼ 10.5) years. However, there were several differences between the two studies which may account for differences in findings. Arnold et al. (2004) included 6 subjects who reported potential vertebrobasilar insufficiency symptoms such as dizziness, blurring of vision and headaches (although these were all negative on physical screening tests). They also included 8 subjects with a history of neck pain and 5 with a history of neck injury. The current study specifically excluded any subjects with such symptoms or history. Arnold et al. (2004)

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Fig. 2. Duplex ultrasound image and spectrogram of the left ICA. Cursor markers on the spectrogram indicate PSV (85.5 cm/s) and EDV (35.6 cm/s).

investigated VA blood flow in six cervical positions with the SMP last in the sequence tested. Another difference is that the SMP was directed at C2/3 in the current study and C1/2 by Arnold et al. (2004). Since the set-up for the SMP involves movement of the neck from the top down to the cervical segment to be manipulated, it is possible that the cervical spine is in a position of greater rotation and side-flexion in the C2/3 SMP than in the C1/2 SMP.

In terms of direction, rotation is generally considered to hold the greatest risk of injury to the VA. The effect of cervical rotation on VA blood flow has yielded conflicting results. However, studies which have demonstrated a significant reduction in VA blood flow velocity contralateral to the direction of rotation (Refshauge, 1994; Licht et al., 1998; Rivett et al., 1999; Mitchell, 2003; Mitchell et al., 2004), and one study which demonstrated a significant increase in VA blood flow velocity ipsilateral to the side of rotation (Licht et al.,

Fig. 3. Duplex ultrasound image and spectrogram of the left VA. Cursor markers on the spectrogram indicate PSV (43.0 cm/s) and EDV (15.2 cm/s).

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Table 1 Effect of cervical spine position on ICA PSV (cm/s), EDV (cm/s), VMean (cm/s) and RI, (group mean  SD). Neutral 1

SMP (LR/RSF)

P valuea

Neutral 2

Left ICA PSV EDV VMean RI

92.36  22.84 33.60  6.81 53.18  11.40 0.63  0.07

95.24  19.15 39.69  9.19 58.21  11.47 0.58  0.07

0.576 0.018** 0.126 0.002**

95.71  20.10 36.00  7.71 55.90  10.52 0.62  0.08

91.21  22.46 32.67  7.60 52.18  11.18 0.63  0.07

0.257 0.253 0.165 0.583

Right ICA PSV EDV VMean RI

98.81  21.73 38.21  6.95 58.41  10.46 0.60  0.07

96.40  19.65 36.26  7.09 56.31  10.09 0.62  0.07

0.484 0.404 0.421 0.342

96.69  17.10 35.86  6.34 56.13  7.34 0.62  0.09

100.62  23.40 37.26  11.32 58.38  13.37 0.62  0.10

0.406 0.476 0.338 0.810

SMP (RR/LSF)

P valuea

LR/RSF ¼ Left Rotation/Right Side-Flexion; RR/LSF ¼ Right Rotation/Left Side-Flexion. **p < 0.05. a Tests the hypothesis that there is no difference between neutral neck position and the SMP.

1998), support the pattern found by Arnold et al. (2004). These authors found a decrease in blood flow velocity in the VA contralateral to the rotation component of the SMP and an increase in blood flow velocity in the VA ipsilateral to the rotation component of the SMP. Since the SMP in the current study includes a greater range of rotation than the study by Arnold et al. (2004), it would be expected that changes in blood flow velocity as a result of the rotation component would be even greater. However, no significant change in blood flow velocity was identified. Threats to validity of the pre-test post-test single group design include history (other events apart from the intervention occurring between measures) and maturation (developments in the group between measures) (Robson, 2002). The group in the current study was isolated sufficiently to ensure that other events did not influence it, however blood flow velocity is dependant on blood pressure. A change in blood pressure between neutral and the SMP, may account for part or all of the differences in blood flow velocity between the two positions. Blood pressure was not measured in this study. However, one study which considered this possibility did not find any correlation between mean blood pressure and PSV (Licht et al., 1998), and in another study, blood pressure did not significantly differ from before to after blood velocity measurements were taken in a series of premanipulative test positions (Rivett et al., 1999). In this study a convenience sample of healthy, asymptomatic individuals was used and no attempt was made to investigate whether the SMP has a greater effect on blood flow in those individuals with positive findings on pre-manipulative testing than in those without such findings. It is therefore not possible to generalise our results to the symptomatic population. Two studies (Licht et al., 2000, 2002) have used subjects with signs or symptoms of neurovascular ischaemia on premanipulative testing, but found no significant differences in VA or ICA blood flow parameters between

various neck positions including neutral, rotation, and combined extension/rotation. Although Rivett et al. (1999) found a significant reduction in PSV in the VA in end-range contralateral rotation and combined rotation/extension in both a positive and healthy group of subjects, they did not find any significant differences between groups. Neither were any significant differences in VA mean velocity ratios measured in rotation, extension and combined extension/rotation found between a positive and healthy group of subjects by Thiel and Yong-Hing (1994). The order in which vessels were measured in the current study was firstly the left ICA followed by the left VA, then the right ICA, and finally the right VA. There could therefore be an order effect which has not been accounted for and future studies should ensure that the order in which vessels are measured is randomized. In addition, the large standard deviation seen in a few of the blood flow parameters indicate that our data would benefit from confirmation of a larger study. Out of all the premanipulative screening tests, the SMP most closely attempts to replicate the mechanical forces to which the ICA/VA are subjected in the position in which a cervical manipulation technique is applied. However, premanipulative positional tests do not test the vessel’s ability to resist the external forces applied during vigorous procedures such as manipulation (Refshauge, 1994). Despite this, the SMP as a screening test could still be useful since the patient’s neck may be held in or near the SMP for some time while the clinician palpates for appropriate segmental ‘locking’ prior to applying a manipulative thrust. The ability to maintain overall cerebral perfusion during this premanipulative period is also important. It has been argued that a negative premanipulative test response does not indicate the real risk of neurovascular complications of neck manipulation (Frisoni & Anzola, 1991; Coté et al., 1996; Di Fabio, 1999; Rivett et al., 1999; Mann & Refshauge,

Table 2 Effect of cervical spine position on VA PSV (cm/s), EDV (cm/s), VMean (cm/s) and RI, (group mean  SD). Neutral 1

SMP (LR/RSF)

P valuea

Neutral 2

SMP (RR/LSF)

P valuea

Left VA PSV EDV VMean RI

55.00  9.47 18.52  3.02 30.68  4.59 0.66  0.05

50.67  11.68 18.29  3.92 29.08  6.33 0.64  0.04

0.233 0.839 0.406 0.027**

57.14  13.71 20.21  4.38 32.52  6.69 0.64  0.07

54.50  14.01 18.95  4.21 30.80  7.01 0.65  0.06

0.391 0.379 0.349 0.808

Right VA PSV EDV VMean RI

54.05  18.73 17.95  5.73 29.98  9.76 0.66  0.06

45.93  8.60 17.45  4.36 26.94  5.27 0.62  0.07

0.097 0.611 0.177 0.043**

53.17  16.27 19.29  6.94 30.58  9.86 0.64  0.06

50.33  15.77 19.52  7.46 29.79  10.10 0.62  0.05

0.219 0.817 0.571 0.027**

LR/RSF ¼ Left Rotation/Right Side-Flexion; RR/LSF ¼ Right Rotation/Left Side-Flexion. **p < 0.05. a Tests the hypothesis that there is no difference between neutral neck position and the SMP.

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2001). Current recommendations therefore place greater weight on the history in clinical decision making rather than a negative test response (Rivett et al., 2006). Non-ischaemic clinical features such as headache and neck pain may be the only warning symptoms of impending dissection, and so careful consideration of the differential diagnosis of these symptoms is recommended (Kerry et al., 2008). A wider assessment of vascular risk factors, such as hypertension, in an individual is also advised (Kerry & Taylor, 2009). Few studies have investigated the link between vascular risk factors and cervical artery dissection (Debette & Leys, 2009), although one study has found an increased prevalence of hypertension in patients with cervical artery dissection (Pezzini et al., 2006). As yet research has not established which risk factors predispose patients to arterial dissection after neck manipulation (Haneline & Rosner, 2007). Nevertheless, the possibility exists for vascular risk factors to render a patient more susceptible to vascular trauma from manipulation of the cervical spine. Further research in this area is clearly needed, but it may be prudent to consider such risk factors in pre-treatment screening. 5. Conclusion The current study set out to investigate the effect of a SMP on blood flow in the ICA and VA in a group of healthy individuals. The results did not provide any evidence that blood flow in this group is adversely affected by placing the cervical spine in a SMP. Our group is currently testing whether the SMP affects ICA and VA blood flow in individuals who have signs or symptoms of neurovascular insufficiency on pre-manipulative testing. Acknowledgment The authors would like to thank Dr Lesley Smith, principal lecturer in quantitative research methods at Oxford Brookes University, for her help with the statistical analysis. References Allan P, McDicken W, Pozniak M, Dubbins P. Clinical doppler ultrasound. Oxford: Churchill Livingstone/Elsevier; 2006. Arnold C & Bourassa, R. Correspondence to Cathy Arnold, Associate Professor, School of Physical Therapy, University of Saskatchewan, [email protected]. 15th December 2008, Personal Communication. Arnold C, Bourassa R, Langer T, Stoneham G. Doppler studies evaluating the effect of a physical therapy screening protocol on vertebral artery blood flow. Manual Therapy 2004;9(1):13e21. Assendelft W, Bouter L, Knipschild P. Complications of spinal manipulation e a comprehensive review of the literature. The Journal of Family Practice 1996;42(5):475e80. Barker S, Kesson M, Ashmore J, Turner G, Conway J, Stevens D. Guidance for premanipulative testing of the cervical spine. Manual Therapy 2000;5(1):37e40. Borghouts J, Koes B, Bouter L. The clinical course and prognostic factors of nonspecific neck pain: a systematic review. Pain 1998;77:1e13. Bronfort G, Nilsson N, Haas M, Evans R, Goldsmith C, Assendelft W, et al. Noninvasive physical treatments for chronic/recurrent headache. Cochrane Database of Systematic Reviews 2004;3. Childs J, Cleland J, Elliott J, Teyhen D, Wainner R, Whitman J, et al. Neck pain: clinical practice guidelines linked to the international classification of functioning, disability, and health from the orthopaedic section of the American physical therapy association. Journal of Orthopaedic & Sports Physical Therapy 2008;38 (9):A1e34. Coté P, Kreitz B, Cassidy D, Thiel H. The validity of the extension-rotation test as a clinical screening procedure before neck manipulation: a secondary analysis. Journal of Manipulative and Physiological Therapeutics 1996;19(3):159e64. Debette S, Leys D. Cervical-artery dissections: predisposing factors, diagnosis, and outcome. The Lancet Neurology 2009;8(7):668e78. Di Fabio R. Manipulation of the cervical spine: risks and benefits. Physical Therapy 1999;79(1):50e64. Ernst E. Cerebrovascular complications associated with spinal manipulation. Physical Therapy Reviews 2004;9(1):5e15. Ernst E. Adverse effects of spinal manipulation: a systematic review. Journal of the Royal Society of Medicine 2007;100(7):330e8.

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