Manual Therapy (2003) 8(2), 103–109 r 2003 Elsevier Science Ltd. All rights reserved. 1356-689X/03/$ - see front matter doi:10.1016/S1356-689X(02)00155-8
Orginal article
The effect of cervical rotation on blood flow in the contralateral vertebral artery C. Zaina*, R. Grantw, C. Johnsonn, B. Dansiez, J. Taylory, P. Spyropolousy Private Practitioner, South Australia, w Division of Health Sciences, University of South Australia, z School of Mathematics, University of South Australia, y Department of Radiology, Royal Adelaide Hospital, South Australia
n
SUMMARY. Twenty asymptomatic volunteers (mean age 33 years, range 26 – 54 years) underwent investigation using duplex Doppler ultrasound with real-time imaging and colour flow enhancement. With the subjects seated, peak velocity at C1-2 and volume flow rate at C5-6 were measured in the artery contralateral to the direction of rotation, in the four positions of neutral, 451 and end range rotation, plus a subsequent neutral position. No change in peak velocity at C1-2 between the initial neutral measurement and the measurements at 451 and end range rotation was found (P>0.05). Peak velocity was less in both vertebral arteries on return to the neutral position as compared with end range rotation, however the difference was significant for the left vertebral artery only (P=0.005). This lends support for the rest period, which is taken between cervical movement tests when conducting pre-manipulative testing, to allow for any latent effect on blood flow of the tests themselves. There was no change in volume flow rate between any of the test positions (P=0.349). There was no indication of a cumulative effect of the test procedure (P>0.05). r 2003 Elsevier Science Ltd. All rights reserved.
indication to a manipulative thrust technique but also to end range passive rotation techniques in treatment. In 1988 following work by Grant (1987, 1988), the Australian Physiotherapy Association formalized a Protocol for Pre-manipulative testing of the cervical spine. Recently, following a survey of manipulative physiotherapists, extensive consultation and consideration of VA blood flow studies, a somewhat modified and expanded set of Clinical Guidelines for Pre-manipulative Procedures of the Cervical Spine (2000) have been developed and accepted by the APA/MPA and represent an evolution of the APA Protocol for Pre-manipulative Testing of the Cervical Spine (1988, Grant 1988). The minimum mandatory movement test under these clinical guidelines is sustained cervical rotation to each side. The effects of sustained rotation on vertebral artery blood flow remain somewhat conflicting (Refshauge 1994, Thiel et al. 1994, Cote et al. 1996, Licht et al. 1998a, b, Rivett et al. 1998, Licht et al. 1999a, b, Licht et al. 2000, Rivett et al. 2000). To an important extent this is dependent upon a number of methodological factors—including whether the method used had established reliability, which blood flow parameter(s) were used, at what level the VA blood flow was measured, which movements and/or combi-
INTRODUCTION Vertebral artery testing has been a part of screening undertaken by physiotherapists for over 30 years. Maitland in 1968 was the first physiotherapist to describe such testing which at that time consisted of sustained cervical rotation to both sides. The onset of dizziness in particular, but any of the symptoms suggestive of VBI, was considered not only a contra-
Received: 9 April 2002 Revised: 14 October 2002 Accepted: 11 December 2002 Cassandra Zaina, B App Sc (Physio), M App Sc (Manip Ther), Clinical Lecturer (part-time), School of Physiotherapy, University of South Australia and Private Practitioner, Adelaide, South Australia, Ruth Grant, Dip Physio BPT, M App Sc, Grad Dip Adv Manip Ther, Pro-Vice Chancellor, Division of Health Sciences, University of South Australia, Catherine Johnson, B App Sc (Physio), M App Sc (Manip Ther), Private Practitioner, Malvern, South Australia, Brenton Dansie, BSc (Hons), PhD, Head, School of Mathematics, University of South Australia, James Taylor, MBBS, FRACR, Department of Radiology, Royal Adelaide Hospital, South Australia, Peter Spyropolous, Assoc Dip Rad Tech, DMU, Department of Radiology, Royal Adelaide Hospital, South Australia. Correspondence to: CZ, 53 Ormond Grove, Toorak Gardens Adelaide, SA 5065, Australia. E-mail:
[email protected] 103
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Critical level
Volume flow rate
Velocity
Increasing stenosis
Fig. 1—The relationship between vessel narrowing, blood velocity and volume flow rate. Modified from Spencer and Reid (1979, p. 329) Reproduced with kind permission of the publishers of Stroke: A Journal of Cerebral Circulation (American Heart Association).
nation of movements were studied, whether one or both vertebral arteries were measured, whether subjects were tested in sitting or supine, whether subjects were symptomatic or asymptomatic, the type of ultrasound equipment used and the level of expertise of the ultrasonographer employed. In 2000, our research group reported the development of a reliable and comprehensive method of measurement of vertebral artery blood flow which incorporated the measurement of peak velocity of blood flow at C1-2, the level of maximum rotation and potential maximum stress on the contralateral vertebral artery, and the measurement of volume flow rate at C5-6 (Johnson et al. 2000). Both measurements should be undertaken to allow a full understanding of the impact of cervical movement on VA blood flow. That is to identify whether a change in peak velocity in the narrowed portion of the VA is sufficient to maintain volume flow rate, or whether the artery is narrowed past the critical level after which changes in blood velocity are unable to maintain a constant volume flow rate and hence blood flow through the vessel is compromized (Spencer & Reid 1979; Zierler 1990; Arbeille et al. 1995). The relationship between these measurements is represented graphically in Fig. 1 (Modified from Spencer & Reid 1979). The current study had the following aims: 1. To investigate the effect of cervical rotation on the peak velocity of blood flow in the contralateral vertebral artery at the level of C1-2. 2. To investigate the effect of cervical rotation on the volume flow rate in the contralateral vertebral artery at the level of C5-6. 3. To investigate whether there was a cumulative effect of the test procedures on these blood flow parameters. r 2003 Elsevier Science Ltd. All rights reserved.
METHOD Ethical approval for this study was granted by the Human Research Ethics Committee of the University of South Australia. Twenty subjects (with a mean age of 32.7 years, SD 8.82 years) were drawn from individuals who volunteered for the study, and who met the essential criteria. Subjects were excluded if they described symptoms of possible VBI origin, cervical pain or stiffness in the preceding 3 months, cardiac problems, pregnancy, known hypotension or hypertension, or were taking medication that may affect blood pressure or haemodynamics of VA flow. Prior to testing, all subjects rested for 15 min to promote haemodynamic stabilization (Brown et al. 1993; Zananiri et al. 1993). Subjects were tested in the sitting position, a position frequently employed clinically for pre-manipulative testing of the cervical spine. Ultrasound evaluation was undertaken using methods previously established to be reliable in our laboratory (Johnson et al. 2000) and using the same ultrasonographer and protocol as in Johnson’s study. This comprised a series of three measurements of peak velocity at C1-2 and a single measurement of volume flow rate at C5-6. (Reliability of these parameters had been previously established—see Johnson et al. 2000; C1-2, ICC of 0.73 deemed ‘fair’ reliability and C5-6, ICC of 0.81 deemed ‘good’ reliability, Blesh 1974). Data were collected for these blood flow parameters in the neutral head position, in 451 rotation and in full range rotation, and on return to neutral head position. These parameters were taken for blood flow in the artery contralateral to the direction of rotation. Both cervical rotations were measured, with the first direction randomly allocated. An ATL colour duplex Doppler HDI 3000 machine with a 7 MHz linear array transducer was used to collect the data.
RESULTS No potential VBI or other symptoms were reported by any subject throughout the procedure. No significant differences were found in the mean diameters of the VAs when comparing left to right, as measured at the level of C5-6 (mean diameter of VA: left= 0.34470.043 cm, right=0.31070.06 cm; P=0.095). The effect of cervical rotation on peak velocity of blood flow in the contralateral VA at C1-2 A repeated measures ANOVA with one within subject factor of repetition was performed for the data sets of the first period (viz. measurements taken in the first direction of rotation), to identify any Manual Therapy (2003) 8(2), 103–109
repetition effect that may have occurred from the three measurements. This was not significant in any position (P>0.05) and hence calculation was continued using the mean of three measurements for peak velocity at C1-2 in each position. Analysis was then undertaken to ascertain whether there was an order effect with respect to rotation. A repeated measures ANOVA with an ‘order’ factor (left rotation followed by right rotation or vice versa) and a ‘period’ factor (first measurement period with first direction of rotation, second measurement period with second direction of rotation) was undertaken along with the main factors of interest, namely the ‘left/right’ rotation factor and a ‘position’ factor (neutral, 451, end of range and neutral). No statistically significant main effects due to order (P=0.19), period (P=0.52) or between order and position (P=0.23) or between period and position (P=0.52) were found. Order and period factors were consequently removed from the analysis and the main factors of interest, namely the direction of cervical rotation and the position of the head, were analysed using a two-factor repeated measures ANOVA. Further analysis revealed that the usual assumptions for applying the ANOVA procedure were more reasonable for the logarithmic data than they were for the raw data, since the distribution against the fitted values was more uniform. Consequently, the remaining analysis was based on ANOVA for the logarithms of peak velocity at C1-2, as the variance is more consistent and independent of velocity for logarithms of peak velocity at C1-2 when compared with the original method, viz. a repeated measures ANOVA using the raw data. Since ‘repetition’ of peak velocity at C1-2 had been shown to have no significant effect, nor had ‘period’ and ‘order’, data were then combined across period and order, and a one-way repeated measures ANOVA with two within subject factors (‘position’ and ‘left/right’) was performed. Head ‘position’ had a significant interaction effect (P=0.027) whilst the interaction between the ‘left/ right’ rotation factor and the ‘position’ factor was close to significance (P=0.056). The means and standard deviations of the logarithms of peak velocity at C1-2 for the left and right VAs in each of the four positions is presented in Fig. 2. This highlights the difference between the left and right VAs in the behaviour of peak velocity at C1-2 in each position. Figure 2 reveals that there was no pattern for peak velocity at C1-2 to increase at 451 of contralateral rotation and decrease at end range contralateral rotation in the left or the right VA. Peak velocity of blood flow was found to be less in both VAs on return to the neutral position as compared with end range rotation, however the difference was significant for the left VA only (P=0.005). This is well illustrated in Fig. 2. Manual Therapy (2003) 8(2), 103–109
Mean logarithms of peak velocity at C1-2 (cm/s)
Effect of cervical rotation 105
Left VA
4.4
Right VA
4.3 4.2 4.1 4 3.9 3.8 3.7 N
45
ER
N
Test Seq uence Fig. 2—The effect of the test sequence on the peak velocity blood flow at C1-2. Means of the logarithms of peak velocity and the standard deviations (Tukey least significant difference) are given for both VAs in N (neutral), 45 (451 contralateral rotation) and ER (end of range contralateral rotation) positions.
The effect of cervical rotation on volume flow rate in the contralateral VA at C5-6 A two-way repeated measures ANOVA was conducted with two between subject factors, namely ‘order’ of rotation and ‘period’ (first rotation compared with the second), and ‘left/right’ (direction of rotation). No significant changes in volume flow rate were demonstrated when considering all interaction factors. Figure 3 illustrates the behaviour of volume flow rate at C5-6 in the VAs with the test sequence. There was no significant change in volume flow rate at C5-6 (P=0.349). It is noted that for the left VA, there is a trend for volume flow rate to decrease at end range however this was not significant. Cumulative effect of the test sequence on peak velocity of blood flow at C1-2 and volume flow rate at C5-6 in the contralateral VAs Cumulative effect was determined by the analysis of the values of these parameters in the three neutral head positions (pre,-mid-and end-test sequence). Two-way repeated measures ANOVAs with one between subject factor of ‘order’ (of rotation) and one within subject factor of ‘neutral 3’ (pre,-mid-and end-test measurements in neutral) of peak velocity at C1-2, and volume flow rate at C5-6 were conducted to determine the presence, if any, of a cumulative effect of repeated rotational positioning on these blood flow parameters. No significant effect of repeated rotation positioning on VA blood flow parameters of peak velocity at C1-2 and volume flow rate at C5-6 was found. r 2003 Elsevier Science Ltd. All rights reserved.
Mean volume flow rate at C5-6 (ml/min)
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Left VA
120 110 100 90 80 70 60 50 40 30 N
45
Right VA
ER
N
Test sequence Fig. 3—The effect of the test sequence on the volume flow rate in the VAs at C5-6 (ml/min). Means for volume flow rate at N (neutral), 45 (451 contralateral rotation) and ER (end of range contralateral rotation) positions are given.
DISCUSSION The relatively recent development of colour Duplex Doppler ultrasound provides the most informative method of sampling blood flow in the vertebral arteries. The relevant current literature is now discussed and results compared with the findings of this study. The effect of cervical rotation on peak velocity of vertebral artery blood flow at C1-2 No significant change in peak velocity in the contralateral artery at C1-2 either at 451 or at end range rotation from the initial pre-test measurement in neutral, was found. The subject sample comprised young asymptomatic volunteers (mean age 32.7 years, SD 8.8 years) and perhaps it is not unexpected to observe a non-significant change in vessel haemodynamics. Comparison with Refshauge’s work (Refshauge 1994) is appropriate, however there are fundamental differences between the studies, so comparisons are made with caution. The differences include the following points. Refshauge sampled peak frequency (a function of peak velocity) at the C2-3 level. This parameter was found to be unreliable and technically difficult to obtain in a study by Johnson et al. (2000)(ICC=0.37). Furthermore, since the measurements were sampled at C2-3, i.e. upstream from the narrowed segment of the VA (viz. C1-2), changes in blood velocity may not be detected. That said, Refshauge’s study was similar to the current study as the subject sample was asymptomatic, and the effect of cervical rotation was assessed using a function of peak velocity of VA flow. Peak velocity at C1-2 for the right VA behaved in a similar fashion to that shown by Refshauge (1994). That is, there was a decrease at 451 and a further decrease at end range rotation. Peak velocity in the r 2003 Elsevier Science Ltd. All rights reserved.
left VA increased at 451 in both studies. At end of range however, the current study showed a further increase in peak velocity, which was not significant, whilst Refshauge (1994) found a significant decrease in velocity. It may be hypothesized that since the supine position was used by Refshauge (1994) as compared to the current study, this may well have provided greater relaxation and permitted a larger range of passive cervical rotation, in turn narrowing the VA sufficiently past the critical level to result in a decrease in blood velocity at end range rotation. Rivett et al. (1999) used the same measurement parameters as Refshauge (1994) and also sampled flow rate parameters at C2-3. These authors investigated the effect of contralateral rotation and combined contralateral rotation/extension on two groups of subjects in supine, one group exhibiting VBI symptoms upon testing, and the other being asymptomatic. Like Refshauge, they found that peak velocity of VA blood flow decreased with contralateral rotation, further decreasing at end range. There was no significant difference between the symptomatic and asymptomatic groups. The 2000 study by Rivett et al. used the same parameters, but this time they sampled at the level of C1-2, in 100 subjects comprising two groups—asymptomatic and symptomatic. Rivett et al. (2000) identified that while the positions of end range contralateral rotation and combined contralateral rotation/extension can occlude the VA, this was not consistently associated with VBI symptoms (only two of 20 patients where partial or complete occlusion of the VA was demonstrated experienced VBI symptoms). Hence these test movements may not predict possible damage to the VAs due to stretching/narrowing with cervical movements. Licht et al. (1998a, b, 1999a, 2000) sampled the VA blood flow in the first part of the VA, specifically between its origin at the subclavian artery and its point of entry into the C6 transverse foramen. This is a suitable site to sample volume flow rate, as there should be minimal morphological alteration to the vessel at this point and consequent turbulence of blood flow which would maximize the reliability of measurement. However, the sampling site is too far upstream to detect changes in velocity of blood flow occurring with narrowing of the VA at C1-2 with cervical rotation. During pre-manipulative testing patients are returned to the neutral cervical position and maintained there for 10 s following each end range test position, to allow for any latent onset of symptoms. Latent symptoms may be a result of altered haemodynamics following the application of the test movements. Partial support was found for this clinical approach in that there was a pattern of reduced peak velocity at C1-2 on return to the neutral position compared with the end range rotation Manual Therapy (2003) 8(2), 103–109
Effect of cervical rotation 107
position for both VAs, however it was significant only for the left VA. A review of the literature has failed to indicate why this decrease in peak velocity may have occurred between end range rotation and the subsequent neutral position in young asymptomatic subjects. The angiographic study of Faris et al. (1963) showed that in some asymptomatic individuals, when a vessel was occluded on contralateral rotation, the vessel failed to fill with blood immediately once returned to the neutral position. However, there was no elaboration as to why this might be so. It could be hypothesized that longitudinal stress applied to the VA at C1-2, such as occurs with end range cervical rotation, results in strain of the elastic fibres within the arterial wall. This may create a creep effect as for other elastic tissue (McGill 1997), hence requiring a period of time to normalize once the stress is released. This would suggest that following rotation, once the neutral position is regained, the lengthened elastic tissue would allow the vessel to expand crosssectionally, until the original elastic fibre length is restored. This would effectively increase the diameter of the VA, with a concomitant reduction in peak velocity. Once the elastic fibres have returned to their original length, the peak velocity would be restored to its original resting value. Further research could elucidate the average time required for peak velocity of VA blood flow to return to pretest levels following sustained contralateral end range rotation. Such research may indicate the optimal rest period required between test positions to ensure that peak velocity of VA blood flow has ‘settled’ prior to undertaking tests in the subsequent positions, or indeed moving on to cervical manipulation or other treatment. The effect of cervical rotation on volume flow rate of vertebral artery blood flow at C5-6 No significant change in volume flow rate at C5-6 was found as a result of cervical rotation. As there was no significant change in peak velocity at C1-2 at full rotation compared with the initial neutral measurement, this is not surprising. These results may indicate that in the healthy, asymptomatic individual, there is minimal change to VA volume flow rate with cervical rotation. It may be the case that greater amounts of rotation are required, such as may occur if the subject is tested in supine rather than sitting, where greater relaxation of the subject may promote increased range of cervical rotation and hence place more stress on the contralateral VA. Alternatively, a combination of cervical movements may be required to further stress the VA, for example, combined rotation/extension. Volume flow rate measurements undertaken by Licht et al. (1999a) in the first part of the VA were Manual Therapy (2003) 8(2), 103–109
conducted with the subject’s head in neutral, in 451 rotation and end-range rotation to either side. These authors found no significant difference in volume flow rate between any cervical positions and this lends support to the findings of the current study. Cumulative effect of the test procedure on vertebral artery blood flow Several authors have raised the possibility of a cumulative effect on blood flow parameters in the VAs with pre-manipulative protocol testing procedures (Terrett 1983; Grieve 1994, Meadows & Magee 1994; Grant 1996). In our laboratory, Schmidt et al. (unpublished) investigated this possibility by sampling peak velocity at C1-2 and volume flow rate at C5-6 before and after the application of the APA Protocol for Pre-manipulative Testing of the Cervical Spine (minus the simulated manipulation position). They found no significant changes in volume flow rate or peak velocity following the application of the pre-manipulative protocol in young asymptomatic volunteers. The current study included this analysis to contribute to the body of knowledge regarding the possibility of a cumulative effect. It must be acknowledged that the test sequence undertaken comprised only a portion of the APA Protocol for Premanipulative Testing of the Cervical Spine (1988) and as such was hypothesized to provide less stress on the VAs and hence a reduced cumulative effect if such existed. However, there were more repetitions of rotational positioning in our test procedures compared with the Protocol (four repetitions, vs one in each direction) and positions were also sustained for a greater period of time due to the requirements of data collection (approximately 90 vs. 10 s hold in the clinical setting). Despite the potential additional stresses on the VAs deriving from the methodology of this current study, no significant difference in peak velocity at C12 or volume flow rate at C5-6 between any of the three neutral measurements was found. This finding identified that the movements of the test sequence provided minimal risk of a cumulative effect upon VA blood flow in this sample of asymptomatic volunteers. Consideration of different patterns of blood flow in the left and right vertebral arteries on rotation The results of this study suggest that with contralateral rotation, the response of peak velocity in the left and right VA may behave differently. Other published research has provided some support for a different pattern of behaviour for blood flow parameters in the left and right VAs but no consistent r 2003 Elsevier Science Ltd. All rights reserved.
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pattern emerges (Refshauge 1994, Stevens 1984; Rivett et al. 1998, 1999). It may be that the size of the VA is a contributing factor, since it is widely documented that the left VA is in general, larger than its counterpart (Scialfa et al. 1975; Cameron & Browning 1982; Thiel et al. 1994; Hedera 1995; Weintraub & Khoury 1995). It is not clear as to why this asymmetry exists, and theories of embryological formation and vascular requirements of the brain have been put forward without evidence. However in the studies where lumen diameter has been reported (Refshauge 1994; Rivett et al. 1998) there was no significant difference between the left and right VAs, yet there was a difference in pattern of blood flow response. In the current study too, although there was a tendency for lumen diameter, peak velocity at C1-2 and volume flow rate at C5-6 to be greater in the left VA compared with its counterpart, there was no significant difference (P=0.095, 0.062 and 0.117 respectively). This suggests that there may be reasons other than vessel size for the different patterns of blood flow within the left and right vessels, and as such could provide a basis for further research.
CONCLUSION In this study of the effects of cervical rotation on blood flow in the contralateral vertebral artery, no significant differences overall were found in the blood flow parameters of peak velocity at C1-2 and volume flow rate at C5-6 at 451 rotation or end range rotation. However, a significant reduction in peak flow velocity at C1-2 in the left VA occurred between end range rotation to the right and return to the neutral position. Although not significant, a similar pattern was evident in the right VA, on return to neutral from left rotation. Whilst this finding needs demonstrating in a sample which includes both symptomatic and asymptomatic subjects it does begin to provide support for the rest period on return to neutral from cervical end range rotation. This rest period of 10 s is a feature of pre-manipulative testing protocols and guidelines and is carried out clinically in order to identify any latent effects of cervical spine positioning. No cumulative effect from repeated rotational positioning on either peak velocity at C1-2 or volume flow rate at C5-6 was found in this young asymptomatic sample. This has clinical relevance given the concerns held by some that the pre-manipulative tests themselves might have a morbid effect on the VAs.
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r 2003 Elsevier Science Ltd. All rights reserved.