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Cervicocephalic Kinesthetic Sensibility in Patients With Chronic, Nontraumatic Cervical Spine Pain George D. Rix, DC, FCC, Jeff Bagust, PhD ABSTRACT. Rix GD, Bagust J. Cervicocephalic kinesthetic sensibility in patients with chronic, nontraumatic cervical spine pain. Arch Phys Med Rehabil 2001;82:911-9. Objective: To investigate cervicocephalic kinesthetic sensibility (head repositioning accuracy to subjective straight ahead) in patients with chronic, nontraumatic cervical spine pain. Design: A prospective, 2-group, observational design. Setting: An outpatient chiropractic clinic in the United Kingdom. Participants: Eleven patients (6 men, 5 women; mean age ⫾ standard deviation, 41.1 ⫾ 13.3yr; range, 18 –55yr) with chronic, nontraumatic cervical spine pain (mean duration, 24 ⫾ 18mo), with no evidence of cervical radiculopathy and/or myelopathy or any other neurologic disorder. Eleven asymptomatic, unimpaired volunteers (5 men, 6 women; mean age, 39.3 ⫾ 10.3yr; range, 28 –54yr) with no history of whiplash or other cervical spine injury or pain served as controls. Main Outcome Measures: Cervicocephalic kinesthetic sensibility was investigated by testing the ability of blindfolded participants to relocate accurately the head on the trunk, to a subjective straight-ahead position, after a near-maximal active movement of the head in the horizontal or vertical plane. The active cervical range of motion and the duration and intensity of neck pain were also recorded. Results: Mann-Whitney U testing indicated that the patient (P) group was no less accurate in head repositioning than the control (C) group for all movement directions except flexion (median global positioning error [95% confidence interval], P ⫽ 5.7° [5.03–9.10], C ⫽ 4.2° [3.17–5.32]; p ⬍ .05). Conclusions: Nontraumatic neck pain patients show little evidence of impaired cervicocephalic kinesthetic sensibility. These results contrast with studies of chronic cervical pain patients in which the origin was not controlled or involved a cervical whiplash injury. Key Words: Cervical vertebrae; Kinesthesis; Proprioception; Neck pain; Rehabilitation. © 2001 by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation ECK PAIN is among the most common and costly health complaints in industrialized society. It is also a common N reason for visits to an accident and emergency department, 1,2
3
and an ambulatory medical provider4; it is the second most common complaint of patients seeking chiropractic care.5-7
From the Department of Academic Affairs, Anglo-European College of Chiropractic, Bournemouth, UK. Accepted in revised form August 22, 2000. Supported by the Anglo-European College of Chiropractic. No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the author(s) or upon any organization with which the author(s) is/are associated. Reprint requests to George D. Rix, DC, FCC, Anglo-European College of Chiropractic, Bournemouth, Dorset, BH5 2DF UK, e-mail:
[email protected]. 0003-9993/01/8207-6272$35.00/0 doi:10.1053/apmr.2001.23300
One study8 reported that as many as 44% of patients with chronic neck pain visit their general practitioner on a yearly basis. There are few reliable epidemiologic studies on the prevalence of chronic neck pain. However, in Norway, Sweden, and Finland, chronic neck pain has been reported in the range of 9.5% to 19.3% for the general population.9-12 Although chronic neck pain can be defined in clinical terms, the underlying pathology and pathophysiology are largely unknown. As with chronic low back pain, research has failed to show a consistent relation between the structural pathology and cervical-related pain.13-21 This has led to a greater awareness of the role of neuromuscular-articular dysfunction in the pathogenesis of neck pain and other syndromes related to the cervical spine.22,23 Recently, attention has been given to the potential role of cervical mechanoreceptive dysfunction in chronic neck pain. In 1991, Revel et al24 introduced a simple test of cervicocephalic sensibility aimed at detecting alterations in cervical proprioception. More specifically, this technique tests the ability of blindfolded subjects to relocate accurately the head to a subjective straight-ahead position, after a maximal active head movement in the horizontal or vertical plane. By using this procedure, several studies found diminished cervicocephalic kinesthesia in chronic neck pain patients in which the cause was not controlled24,25 or specifically involved a cervical whiplash injury.26,27 By using a different measuring technique, a similar loss of kinesthetic sensibility was found in chronic whiplash patients when they were asked to relocate their head to various rotation and side-bending positions.28 Although the cervical facet joint capsules contain a significant density and distribution of different mechanoreceptors,29 it is the small intrinsic muscles30-32 (particularly deep suboccipital muscles) that are likely to have a primary role in signalling the cervical proprioceptive information involved in the conscious perception of equilibrium, position, and spatial orientation when vision is occluded.29,33,34 Hence, one explanation for the diminished kinesthesia findings, in both groups of chronic neck pain patients, involves a functional alteration in the muscle spindle receptors.24 This functional deficit could occur as a result of muscle pain35,36 as well as articular pain and dysfunction.37-39 The cervical facet joints have been documented as a source of nociception in chronic neck pain, particularly after a cervical injury such as whiplash.40-44 However, it has been suggested that atrophy and fatty infiltration in the deep suboccipital muscles may lead to diminished or altered proprioceptive input to higher centers,45,46 as evidenced by a reduced standing balance performance.47 These findings again may be the result of chronic nociception, inhibition from articular dysfunction, or simply from disuse. However, in a patient with chronic neck pain and suboccipital atrophy after a forced flexion cervical injury, electromyography and magnetic resonance imaging abnormalities provided some evidence of denervation, possibly as a result of nerve damage from trauma to the C1 dorsal ramus.48 The existence of muscle pain in spinal pain syndromes is controversial.49 With respect to chronic neck pain of traumatic and nontraumatic origins, relatively little research has explored muscle tissue as a source of pain and dysfunction. There is Arch Phys Med Rehabil Vol 82, July 2001
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some evidence to suggest that there are overlaps in the underlying muscle pathology and pathophysiology in different origins of chronic neck pain.50,51 However, in whiplash injury, in addition to possible functional disturbances in muscle mechanoreception as a result of muscle pain and or facet/facet capsular insult, the potential exists for extrafusal muscle fiber damage.52 Although there is no direct evidence, it is reasonable to suspect that this potential damage and inflammation may also include damage and alteration in function of the muscle spindles and associated receptor endings. Because cervicocephalic kinesthetic sensibility has not been investigated specifically in patients with no history of cervical spine trauma,24-28 the question arises whether these patients have the same degree of diminished kinesthetic sensibility as patients who have chronic neck pain as a result of whiplash trauma.26-28 This preliminary study compared head repositioning accuracy (subjective straight-ahead) in patients with chronic, nontraumatic cervical spine pain with a control group matched for age and gender. METHODS Study Design This study took place in the outpatient clinic at the AngloEuropean College of Chiropractic (AECC), in Bournemouth, UK. A prospective, 2-group design with repeated measures was used. Completion of questionnaires and all measurement procedures were conducted in the same room on each occasion. Subject Selection Patients in the study were selected from all patients presenting for the first time to the AECC clinic over a 6-week period. All new patients completed a simple questionnaire as part of the inclusion-exclusion procedure. On daily review of these first stage questionnaires, the clinical records of patients who provisionally met the inclusion criteria were subjected to secondary detailed screening by an experienced member of the chiropractic faculty. After this screening, subjects who met the inclusion-exclusion criteria (table 1) were contacted by telephone and invited to participate in the study. Patients willing to participate met with the examiner before their first chiropractic
Table 1: Inclusion and Exclusion Criteria Inclusion 1. Age 18–55yr 2. Men and women 3. Continuous neck pain of more than 7wk 4. Neck pain as main presenting complaint Exclusion 1. Onset of presenting neck pain episode after trauma (eg, whiplash) 2. History of cervical injury of trauma since the onset of presenting neck pain episode 3. History of cervical injury or trauma 4. Cervical radiculopathy and/or myelopathy 5. Inflammatory arthritis involving C-spine 6. Tumor or infection involving C-spine 7. Vertebrobasilar artery insufficiency 8. Neurologic disease (eg, multiple sclerosis, Parkinson’s disease, syringomyelia) 9. Congenital anomalies involving the C-spine 10. Systemic disease (eg, diabetes mellitus) Abbreviation: C-spine, cervical spine.
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treatment session, were given further verbal and written information about the study, and were asked to read and sign a consent form. The control subjects were recruited from AECC staff, faculty, and students after they responded to a screening questionnaire. To be considered for inclusion, the subjects must have been aged 18 to 55 years, have had no history of whiplash or other cervical spine injury or pain, have had no history of dizziness or vertigo, have been under no treatment for any other musculoskeletal complaint, and have had no systemic disease or any of the conditions listed under the exclusion criteria in table 1. Finally, eligible control subjects were selected by age and gender to ensure a similar distribution to the patient group. Outcome Measures Clinical characteristics of the neck pain group. The main variables collected for each patient were the following: the current intensity of pain, as rated by an 11-point numeric rating scale; duration and evolution of pain; and the unilateral or bilateral localization of pain through drawings. Other psychometric data considered conceptually important aspects of neck pain, and that are commonly measured, were gathered through the Bournemouth Questionnaire,53 with modifications for neck pain patients. Active range of cervical motion. A cervical range-of-motion (CROM) devicea was used to assess cervical motion in the transverse (rotation), sagittal (flexion-extension), and frontal (lateral-bending) planes. Several studies have shown that the device has acceptable reliability in measuring range of motion (ROM).54,55 The equipment consists of a magnetic yoke that rests on the shoulders and a plastic headpiece with 3 goniometers positioned to measure the 3 cardinal planes of movement. The transverse plane measurement involves a compass goniometer and the magnetic yoke. Measurement of sagittal and frontal plane motion was by gravity goniometers. The same CROM instrument was used throughout the study. Kinesthetic sensibility test. Cervicocephalic kinesthetic sensibility (head repositioning accuracy [HRA]) was measured using a simple clinical technique adapted from the method described by Revel et al.24 This technique requires subjects to have their vision occluded and to wear a light headpiece that is strapped firmly to the head. A laser pointer is fixed to the top of the helmet aimed at a target 90cm in front of the subject. We used a cycling helmetb fitted with a laser pointer (total weight, 375g) and a sleeping mask to occlude the vision (fig 1). A square target holder was constructed (40 ⫻ 40cm) that slotted into the filter holder on the front of a radiograph tube. Targets were made from 40 ⫻ 40cm sheets of graph paper, ruled with 1-mm resolution gridlines. Horizontal (x) and vertical (y) axes were drawn on the paper so that they intersected at the midpoint, dividing the paper into 4 quadrants. The point of intersection was used as the reference zero (coordinates, 0,0) position on the target. The mobility of the tube in x, y, and z directions enabled the target’s 0 point to be accurately centered to the subject’s reference head position. Measurement Protocol All measurement procedures were conducted by the same examiner, a chiropractor with 5 years of clinical experience. On arrival, patients were asked to complete questionnaires. Because the control group was recruited a few weeks before the measurement session, they were checked again to ensure that they met inclusion-exclusion criteria. For both the CROM instrument and HRA measurements, the subjects were seated in a chair with a backrest for the lumbar and lower thoracic
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repositioning to reference 0, in the sagittal plane, from a near-maximal Ext movement (Ext f 0) of the head for 10 repetitions and from a near-maximal Flex movement (Flex f 0) for 10 repetitions. The same sequence of movements was used for all subjects.
Fig 1. Experimental apparatus and testing procedure used to evaluate cervicocephalic kinesthetic sensibility.
regions only. They sat as far back in the chair as possible with their arms hanging by their sides, and the rear of their heels placed against specific foot markings on the floor. They were told that the target would be straight ahead but would be fitted and moved into position only after they were blindfolded. The CROM device was then fitted to the head. For the half-cycle ROM measurements, subjects assumed a neutral, straightahead posture with the head. Motion was measured in the following order for all participants: left rotation (LR), right rotation (RR), extension (Ext), forward flexion (Flex), and left then right lateral flexion (LLF, RLF). The measurement routine was repeated 3 times and a mean score calculated for each motion direction. Movement directions that were painful for the patient group were also recorded. The CROM instrument was then removed. Next, the HRA testing procedure and objectives were again explained to the subjects, who then had their vision occluded with a sleeping mask for the remainder of the procedure. All were instructed to keep their eyes closed behind the mask. The cycling helmet was then firmly secured to the head with the chinstrap. After the target was positioned, room lights were dimmed, and subjects were asked to put their head into what they perceived to be a straight-ahead position. They were told to memorize this position and then relocate their head back to it after a single near-maximal amplitude extension movement of the head. Subjects were told that this was the reference 0 position and that they were to relocate back to this position as accurately as possible after each movement. The target was then moved so that the laser pointer’s beam projected on the 0 of the target. After concentrating for a few seconds on this reference position, subjects were instructed to perform a nearmaximal rotation of the head to the left (LR) and then immediately to relocate back to the reference 0 position with maximum precision. No speed instruction was given. The point where the light beam stopped on the target was marked with a pen dot and labeled according to the repetition number. Ten repetitions of HRA to reference 0 were done with this LR movement (LR f 0), followed immediately by 10 repetitions of HRA to reference 0 with a near-maximal RR movement (RR f 0). After approximately 2 minutes’ rest, a new reference 0 position was established after a single near-maximal amplitude LR movement of the head (with a new adjustment of the target 0 position). The same HRA procedure was then used to test
Data Analysis The main variables compared for differences between the patient and control groups were age, gender, active CROM, and HRA. After testing for normal distribution (AndersonDarling test56), age differences were studied with a MannWhitney U test. Differences in gender distribution between the 2 groups were compared using a chi-square test. The active CROM data were normally distributed, and therefore differences between the groups were studied using an unpaired t test (1-tailed). For HRA, the projection on the abscissa and ordinate axes were measured (X, Y), and each coordinate was given a positive or negative value according to its position relative to the corresponding axis. Using these 2 values, the subject’s global HRA (R) in centimeters was then calculated trigonometrically. This measurement represented the direct distance between the point on which the light beam stopped on the target to the 0 point (center) of the target (fig 2). For every subject, mean values of the 10 repetitions were then calculated for each HRA movement to reference 0 to allow comparisons of differences between groups. Using the distance between the beam on the top of the helmet and the target, these mean centrimetric displacements of the light beam on the target were converted into angular head displacements in degrees. These data, with positive and negative signs, were used to examine undershoot and overshoot characteristics between the groups. Because these data were found to be normally distributed (Anderson-Darling test), differences were studied using an unpaired t test (2-tailed). To allow comparison of the absolute
Fig 2. HRA data collection on target and initial analysis. Point 0 represents the center of the target (coordinates 0,0), which is aligned with the projection of the light beam from the subject’s reference 0 position. Point R indicates the position that the light beam stopped when the head was repositioned after a near-maximal movement. The distance 0 –R converted into degrees represents the global error of positioning (R). The horizontal projection (0 –X) and the vertical projection (0 –Y) indicate the horizontal and vertical components of the global error.
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values for the horizontal (X) and vertical (Y) components of the repositioning error, the negative signs were removed by calculating the root mean square values. This converted HRA data did not display a normal distribution (Anderson-Darling test), and therefore differences between the 2 groups in the absolute R, X, and Y measurements was studied using a MannWhitney U test. Correlations between HRA and age, intensity, and duration of pain were investigated with Spearman’s rank-order correlation using MINITAB威 12 statistical software.c Values of p less than .05 were considered statistically significant. RESULTS Group Demographics and Clinical Characteristics Over the 6-week study period, 15 new patients fulfilled the inclusion-exclusion criteria, but only 11 were willing and able to participate. This cervicalgic group included 11 subjects (6 men, 5 women) between the ages 18 and 55 years (mean age ⫾ standard deviation, 41.1 ⫾ 13.3yr). Eleven healthy subjects (5 men, 6 women) between 28 and 54 years old (mean age, 39.3 ⫾ 10.3yr) were recruited as control subjects. No significant differences were shown for any of these variables between the 2 groups. Data from the neck pain questionnaire profiled the cervicalgic characteristics for the patient group. In all cases, the subjects described their neck pain pattern as daily or continuous. Duration of their pain ranged from 3 months to 5 years, with a mean of 24 ⫾ 18 months. The average intensity of the pain on the day of the examination was 5.1 ⫾ 1.9 points (range, 2– 8). Four patients (36%) reported their neck pain as predominantly left sided, 6 (55%) reported it as bilateral or central, and 1 (9%) reported it as right sided. Active CROM Figure 3 shows that when compared with the control subjects, the patient group had a decreased active CROM in each of the 6 motion directions. Unpaired t tests (1-tailed) showed a significant difference between the 2 groups for RR (mean for patients, 61.5° ⫾ 7.9°; mean for controls, 69.6° ⫾ 8°; p ⬍ .05); Flex (mean for patients, 44.5° ⫾ 10.9°; mean for controls, 54.1° ⫾ 8.1°; p ⬍ .05); and LLF (mean for patients, 33.1° ⫾ 12.5°; mean for controls, 41.6° ⫾ 5.5°; p ⬍ .05). Kinesthetic Sensibility HRA: absolute values. An overview of the mean values of the 10 repositioning repetitions, in each of the 4 movement
Fig 3. Active CROM measurements in neck pain (black bar) and control (gray bar) subjects. All data are mean ⴞ standard error of the mean.
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directions, is presented in scatterplots in figure 4. Table 2 presents the median values for global (R), absolute horizontal (X), and vertical (Y) repositioning errors (degrees) in the neck pain patients and control subjects. Mann-Whitney U tests showed that there were no significant differences within the control group for the median global HRA values and the absolute values for the X and Y components for all 4 movement directions. However, within the patient group, a significant difference was shown between the median global HRA values for RR f 0 versus LR f 0 (p ⬍ .01) and RR f 0 versus Ext f 0 (p ⬍ .01). Mann-Whitney U tests (table 2) revealed no significant difference between groups in the median global HRA values and the absolute median X and Y components for LR f 0, RR f 0, and Ext f 0. For the Flex f 0 trial, the patient group showed a significantly higher global repositioning error compared with the controls (p ⬍ .05). Most of this difference occurred within the Y component of the repositioning error, although significance was not reached (p ⫽ .07). Characteristics of HRA. For the Ext f 0 and Flex f 0 trials, analysis of the X and Y components showed that for both groups, the absolute repositioning error was greater in the movement plane than in the perpendicular plane (table 2). For the LR f 0, RR f 0 trials, this relationship was only seen in the patient group, and a reverse pattern was seen in the control group. Table 3 presents the data used for overshoot-undershoot error analysis. One-sample t tests, used to compare the means to reference 0, showed no significant overshoot-undershoot tendencies in the control group for any of the repositioning directions. Within the patient group, a significant overshoot was found for Flex f 0 in the Y plane (p ⬍ .05). Unpaired t tests showed that there were no significant differences between the groups (table 3). Variability of HRA with repetitions. Analysis of the data for both groups (Mann-Whitney U tests) showed no trends in the HRA suggestive of learning interference, fatigue, drop in the attention span, or other such phenomena. Throughout the series of repetitions for each of the repositioning movements, there were no trends or significant differences. Interestingly, for both groups, any error of head repositioning usually occurred with the first of the 10 repetitions. No significant deviation from this relocation point was found with the remaining 9 series of repositionings. One-way analysis of variance tests (with Fisher’s least significant difference post hoc tests) showed no significant differences in overshoot-undershoot tendencies throughout each series of repetitions. Correlation of clinical variables with HRA. There was no evidence of correlation between head repositioning error and age for either of the study groups, nor was there any correlation between head repositioning error in the neck pain group and pain characteristics (pain intensity on day of examination, duration of pain, localization of pain, painful movement). DISCUSSION This preliminary study focused on cervicocephalic kinesthetic sensibility in a subgroup of patients with chronic neck pain of nontraumatic origin. More specifically, we examined subjects’ ability to return the head to a subjective straightahead position after an active movement away from this point. This method has been used in several studies.24-27 Results from our limited sample did not indicate a general reduction in HRA in the neck pain group when compared with the unimpaired controls. Our results contrast with studies involving chronic cervical pain patients in which the cause was not controlled24 or involved a cervical whiplash injury.26,27 We did find, however,
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Fig 4. Scatterplots showing the HRA for the neck pain and control subjects. All data are presented as degrees. Abbreviations: HRA to reference 0 after a near-maximal active head movement: LR f 0, left rotation; RR f 0, right rotation; Ext f 0, extension; Flex f 0, flexion.
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Table 2: Global (R), Absolute Horizontal (X), and Vertical (Y) Repositioning Error (deg) in Neck Pain Patients and Control Subjects Neck Pain Patients
LR
R X Y R X Y R X Y R X Y
RR
Ext
Flex
Control Subjects
Median (95% CI)
Mean
Median (95% CI)
Mean
p*
3.7 (3.10–5.80) 1.9 (1.38–2.95) 1.9 (.96–3.28) 6.1 (5.84–8.69) 4.8 (3.17–8.12) 3.2 (2.18–4.82) 4.3 (3.49–5.72) 1.0 (.38–3.40) 3.8 (2.83–4.63) 5.7 (5.03–9.10) 1.1 (.39–2.52) 4.9 (3.04–9.10)
4.2 2.3 2.0 6.9 5.2 3.3 5.2 1.6 4.4 6.3 1.6 5.4
4.0 (2.50–6.34) 1.4 (.30–4.40) 2.1 (1.15–3.88) 6.0 (1.41–12.31) 3.6 (.85–11.93) 2.6 (.68–4.51) 5.1 (2.83–7.14) 1.3 (.20–2.04) 2.9 (1.57–6.75) 4.2 (3.17–5.32) 2.2 (1.29–3.22) 3.1 (2.19–4.82)
4.5 2.5 2.7 6.0 4.8 2.5 5.1 1.5 4.2 4.6 2.7 3.5
NS NS NS NS NS NS NS NS NS ⬍.03 NS NS
Abbreviations: CI, confidence interval; NS, not significant. * Differences not significant using Mann-Whitney U tests on median values (p ⬎ .05).
a statistically significant reduced global HRA (R) in the neck pain group for the Flex f 0 trial, with a tendency for overshooting the reference 0 position. However, the lack of distinct separation of the data displayed in the scatterplots (fig 4) would suggest that this may have limited clinical meaning. The method we used to measure cervicocephalic kinesthetic sensibility is a relatively simple equipment design that is inexpensive, easy to execute, and may permit a degree of discriminant classification of certain cervicalgic subgroups. Although some data are available showing a reasonable reproducibility26 and consistency between similar neck pain populations,24,25 the method of measurement and, in particular, its subjective and nonremote nature inevitably involve a degree of experimenter bias and geometric inaccuracy. On this basis, comparing absolute values between different studies should be done with caution. The method we used differed slightly from that used previously in that our subjects were asked to perform a nearmaximal movement of the head instead of a maximal amplitude head movement. Our rational for this was that most of the neck pain subjects experienced a sharp increase in pain at the end ROM, which we felt may have biased their repositioning ability. It was also apparent during our pilot trials that when subjects were asked to turn their head maximally, there was a degree of shoulder and trunk rotation that we believed needed to be eliminated to maintain neck isolation. The significance of this difference in method needs to be explored in future studies. Table 3: Overshoot and Undershoot Characteristics Relative to the Target’s Center (Reference 0) for the 2 Groups Neck Pain Patients
LR RR Ext Flex
X Y X Y X Y X Y
Control Subjects
Mean ⫾ SD
Mean ⫾ SD
p*
⫺1.3 ⫾ 2.5 ⫺1.0 ⫾ 2.3 ⫺1.1 ⫾ 6.2 ⫺1.5 ⫾ 3.4 ⫺0.5 ⫾ 2.1 ⫺0.5 ⫾ 5.6 ⫺0.4 ⫾ 2.1 4.0 ⫾ 5.1
⫺1.2 ⫾ 3.4 ⫺1.7 ⫾ 2.7 0.2 ⫾ 7.3 ⫺1.6 ⫾ 2.8 0.3 ⫾ 2.2 1.5 ⫾ 4.9 1.6 ⫾ 3.4 1.3 ⫾ 4.0
NS NS NS NS NS NS NS NS
Abbreviation: SD, standard deviation. * Differences not significant using a unpaired t test (2-tailed) on mean values (p ⬎ .05).
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Another possible inconsistency arises when we consider the active head movement used to obtain the reference 0 position of the target. Previous studies do not describe in which direction this reference movement was made.24-27 We chose a consistent perpendicular movement for each of the horizontal and vertical movement trials. A limited examination of our data did not indicate that there was any contamination of head repositioning error between the movement planes, but further investigation of the effect on the HRA of the preliminary movement may be warranted. The cervical kinesthetic test used in this and earlier studies is thought to examine primarily cervical spine kinesthetic performance.24 The integrated nature and functional overlap of the various sensory inputs within the systems involved in equilibrium, spatial, and self-motion awareness make isolation of a single subsystem, such as the cervical mechanoreceptive apparatus, difficult. Theoretically, a procedure involving movement of the trunk only, with the head stationary in space, would seem to be the most useful method of producing a pure neck stimulus.57,58 The head repositioning test measures a subject’s ability to relocate the head to a specific subjective straight-ahead position after an active head movement away from that position. This involves an appreciation of both position and movement of the head in space. Because the head cannot move without movement in the cervical spine, and a subjective straight-ahead orientation is the reference point, this procedure also involves spatial and movement awareness of the head relative to the trunk. In this experiment, the subjects were seated and blindfolded, and the trunk and limbs were kept stationary. This procedure potentially involves head-in-space information from the vestibular system and head-on-trunk proprioceptive information from the cervical spine mechanoreceptors.57,59,60 Results of studies in which subjects graded their perception of various movements suggest that the head movements in this and previous studies24-27 may use peripheral kinesthetic information primarily from the cervical spine mechanoreceptive apparatus.57 Added to this is evidence suggesting that this may only be the case at low speed head movements.57 As no speed instructions were given during our testing procedure, the possibility exists that we found no meaningful differences because the active movements were conducted too rapidly. However, because it is believed that most of the tonic neuronal component (corresponding to head position) in the test procedure can be identified as cervical,58 the rate of head movement may not be a methodologic issue. The effect of head
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movement speed on cervicocephalic kinesthetic sensibility should be evaluated further. Assuming that our method was adequate for detecting any reduction in cervicocephalic kinesthetic sensibility, what then could be the meaning of the lack of any obvious reduction in HRA in this small sample of chronic, nontraumatic neck pain subjects? The functional and relevant structural pathology of the cervical spine underlying chronic mechanical neck pain remains largely unclear.61-64 However, when considering the pathogenesis of chronic mechanical neck pain, 2 models of neck pain and dysfunction are commonly seen. They are the so-called idiopathic (nontraumatic) neck pain and neck pain directly attributable to a cervical spine trauma (eg, whiplash injury). This division may seem somewhat artificial if we consider that the clinical presentation, dysfunction, and structural pathology of patients in both subgroups and with other origins often have much in common.44,47,48,50,62-65 CONCLUSION The results of our study indicate that, with respect to HRA to a subjective straight-ahead position, there may be a division between the 2 subgroups. This may reflect some differences in the underlying cervical spine dysfunction. Although many tissues in the cervical spine contain various mechanoreceptive nerve endings,29,33,66 most of the cervical proprioceptive information involved in the conscious perception of equilibrium, position, and spatial orientation when vision is occluded is probably derived from muscle receptor afferents.33,34,67-72 The most dense population of muscle spindles has been found in the small intrinsic muscles,30-32,73,74 and atrophy of some of these muscles has been linked to a loss of standing balance.47 It is, therefore, reasonable to conclude that changes in HRA could result from structural pathology or alteration in the function of these spindle-rich muscles, either primarily47,48,50 and/or secondary to muscle pain,35,36,75-79 ligamentous injury,80-86 articular pain,37 and articular dysfunction.38,39,87 It may also be that in some aspects this neuromuscular dysfunction may differ between patients with neck pain directly related to cervical spine trauma and patients with so-called idiopathic neck pain. However, as diminished HRA has been found in studies involving chronic neck pain patients in which the origin was not controlled,24,25 this conclusion may be premature. Acknowledgment: The authors thank Ian Brown, PhD, for his assistance in development of the protocol, Angelu Wood, DSR, SRR, for use of the radiography room, and Kim Humphreys, DC, PhD, FCC, and Haymo Thiel, MSc, DC, FCC, for screening the new patients for eligibility. References 1. Clark W, Haldeman S. The development of guideline factors for the evaluation of disability in neck and back injuries. Division of Industrial Accidents, State of California. Spine 1993;18:1736-45. 2. Borghouts JA, Koes BW, Vondeling H, Bouter LM. Cost-ofillness of neck pain in The Netherlands in 1996. Pain 1999;80: 629-36. 3. Stussman BJ. National hospital ambulatory medical care survey: 1993 emergency department summary. Adv Data 1996;271:1-15. 4. Schappert SM. National ambulatory medical care survey: 1994 summary. Adv Data 1996;273:1-18. 5. Shekelle PG, Brook RH. A community-based study of the use of chiropractic services. Am J Public Health 1991;81:439-42. 6. Hurwitz EL, Coulter ID, Adams AH, Genovese BJ, Shekelle PG. Use of chiropractic services from 1985 through 1991 in the United States and Canada. Am J Public Health 1998;88:771-6. 7. Pedersen P, Noddeskou H, Wejse B. A pilot survey of diagnoses, radiographic and laboratory procedures encountered in European chiropractic practices. Eur J Chiropractic 1992;40:71-82.
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8. Borghouts J, Janssen H, Koes B, Muris J, Metsemakers J, Bouter L. The management of chronic neck pain in general practice. A retrospective study. Scand J Prim Health Care 1999;17:215-20. 9. Andersson HI, Ejlertsson G, Leden I, Rosenberg C. Chronic pain in a geographically defined general population: studies of differences in age, gender, social class, and pain localization. Clin J Pain 1993;9:174-82. 10. Brattberg G, Thorslund M, Wikman A. The prevalence of pain in a general population. The results of a postal survey in a county of Sweden. Pain 1989;37:215-22. 11. Bovim G, Schrader H, Sand T. Neck pain in the general population. Spine 1994;19:1307-9. 12. Makela M, Heliovaara M, Sievers K, Impivaara O, Knekt P, Aromaa A. Prevalence, determinants, and consequences of chronic neck pain in Finland. Am J Epidemiol 1991;134:1356-67. 13. Gore DR, Sepic SB, Gardner GM. Roentgenographic findings of the cervical spine in asymptomatic people. Spine 1986;11:521-4. 14. Heller CA, Stanley P, Lewis-Jones B, Heller RF. Value of x-ray examinations of the cervical spine. Br Med J (Clin Res Ed) 1983;287:1276-8. 15. Boden SD, McCowin PR, Davis DO, Dina TS, Mark AS, Wiesel S. Abnormal magnetic-resonance scans of the cervical spine in asymptomatic subjects. A prospective investigation. J Bone Joint Surg Am 1990;72:1178-84. 16. Friedenberg ZB, Miller WT. Degenerative disc disease of the cervical spine: a comparative study of asymptomatic and symptomatic patients. J Bone Joint Surg Am 1963;45:1171-8. 17. Liebenson CS. Pathogenesis of chronic back pain. J Manipulative Physiol Ther 1992;15:299-308. 18. Marchiori DM, Henderson CN. A cross-sectional study correlating cervical radiographic degenerative findings to pain and disability. Spine 1996;21:2747-51. 19. Pettersson K, Hildingsson C, Toolanen G, Fagerlund M, Bjornebrink J. MRI and neurology in acute whiplash trauma. No correlation in prospective examination of 39 cases. Acta Orthop Scand 1994;65:525-8. 20. Karlsborg M, Smed A, Jespersen H, Stephensen S, Cortsen M, Jennum P, et al. A prospective study of 39 patients with whiplash injury. Acta Neurol Scand 1997;95:65-72. 21. Ronnen HR, de Korte PJ, Brink PR, van der Bijl HJ, Tonino AJ, Franke CL. Acute whiplash injury: is there a role for MR imaging?—a prospective study of 100 patients. Radiology 1996;201: 93-6. 22. Lewit K. The functional approach. J Orthop Med 1994;16(3):73-4. 23. Murphy DR. Dysfunction in the cervical spine. In: Murphy DR, editor. Conservative management of cervical spine syndromes. New York: McGraw-Hill; 2000, p 71-103. 24. Revel M, Andre-Deshays C, Minguet M. Cervicocephalic kinesthetic sensibility in patients with cervical pain. Arch Phys Med Rehabil 1991;72:288-91. 25. Revel M, Minguet M, Gergoy P, Vaillant J, Manuel JL. Changes in cervicocephalic kinesthesia after a proprioceptive rehabilitation program in patients with neck pain: a randomized controlled study. Arch Phys Med Rehabil 1994;75:895-9. 26. Heikkila H, Astrom PG. Cervicocephalic kinesthetic sensibility in patients withwhiplash injury. Scand J Rehabil Med 1996;28: 133-8. 27. Heikkila HV, Wenngren BI. Cervicocephalic kinesthetic sensibility, active range of cervical motion, and oculomotor function in patients with whiplash injury. Arch Phys Med Rehabil 1998;79: 1089-94. 28. Loudon JK, Ruhl M, Field E. Ability to reproduce head position after whiplash injury. Spine 1997;22:865-8. 29. McLain RF. Mechanoreceptor endings in human cervical facet joints. Spine 1994;19:495-501. 30. Wilson VJ. Physiologic properties and central actions of neck muscle spindles. In: Berthoz A, Vidal P, Graf W, editors. The head-neck sensory motor system. New York: Oxford Univ Pr; 1992. p 175-8. 31. Nitz AJ, Peck D. Comparison of muscle spindle concentrations in large and small human epaxial muscles acting in parallel combinations. Am Surg 1986;52:273-7. Arch Phys Med Rehabil Vol 82, July 2001
918
CERVICOCEPHALIC KINESTHETIC SENSIBILITY, Rix
32. Richmond FJ, Bakker DA. Anatomical organization and sensory receptor content of soft tissues surrounding upper cervical vertebrae in the cat. J Neurophysiol 1982;48:49-61. 33. Bolton PS. The somatosensory system of the neck and its effects on the central nervous system. J Manipulative Physiol Ther 1998; 21:553-63. 34. Proske U, Schaible HG, Schmidt RF. Joint receptors and kinaesthesia. Exp Brain Res 1988;72:219-24. 35. Matre DA, Sinkjaer T, Svensson P, Arendt-Nielsen L. Experimental muscle pain increases the human stretch reflex. Pain 1998;75: 331-9. 36. Pedersen J, Sjolander P, Wenngren BI, Johansson H. Increased intramuscular concentration of bradykinin increases the static fusimotor drive to muscle spindles in neck muscles of the cat. Pain 1997;70:83-91. 37. Schaible HG, Grubb BD. Afferent and spinal mechanisms of joint pain. Pain 1993;55:5-54. 38. Hurley MV, Jones DW, Newham DJ. Arthrogenic quadriceps inhibition and rehabilitation of patients with extensive traumatic knee injuries. Clin Sci (Colch) 1994;86:305-10. 39. Hurley MV, Scott DL, Rees J, Newham DJ. Sensorimotor changes and functional performance in patients with knee osteoarthritis. Ann Rheum Dis 1997;56:641-8. 40. Bogduk N, Marsland A. The cervical zygapophysial joints as a source of neck pain. Spine 1988;13:610-7. 41. Lord SM, Barnsley L, Wallis BJ, Bogduk N. Chronic cervical zygapophysial joint pain after whiplash. A placebo-controlled prevalence study. Spine 1996;21:1737-44; discussion 1744-5. 42. Aprill C, Bogduk N. The prevalence of cervical zygapophyseal joint pain. A first approximation. Spine 1992;17:744-7. 43. Ketroser DB. Whiplash, chronic neck pain, and zygapophyseal joint disorders. A selective review. Minn Med 2000;83:51-4. 44. Barnsley L, Lord SM, Wallis BJ, Bogduk N. The prevalence of chronic cervical zygapophysial joint pain after whiplash. Spine 1995;20:20-5; discussion 26. 45. McPartland JM, Brodeur RR. Rectus capitis posterior minor: a small but important suboccipital muscle. J Bodywork Move Ther 1999;3(1):30-5. 46. Hallgren RC, Greenman PE, Rechtien JJ. Atrophy of suboccipital muscles in patients with chronic pain: a pilot study. J Am Osteopath Assoc 1994;94:1032-8. 47. McPartland JM, Brodeur RR, Hallgren RC. Chronic neck pain, standing balance, and suboccipital muscle atrophy—a pilot study. J Manipulative Physiol Ther 1997;20:24-9. 48. Andary MT, Hallgren RC, Greenman PE, Rechtien JJ. Neurogenic atrophy of suboccipital muscles after a cervical injury: a case study. Am J Phys Med Rehabil 1998;77:545-9. 49. Bogduk N. The anatomical basis for spinal pain syndromes. J Manipulative Physiol Ther 1995;18:603-5. 50. Uhlig Y, Weber BR, Grob D, Muntener M. Fiber composition and fiber transformations in neck muscles of patients with dysfunction of the cervical spine. J Orthop Res 1995;13:240-9. 51. Weber BR, Uhlig Y, Grob D, Dvorak J, Muntener M. Duration of pain and muscular adaptations in patients with dysfunction of the cervical spine. J Orthop Res 1993;11:805-10. 52. Brault JR, Siegmund GP, Wheeler JB. Cervical muscle response during whiplash: evidence of a lengthening muscle contraction. Clin Biomech (Bristol) 2000;15:426-35. 53. Bolton JE, Breen AC. The Bournemouth Questionnaire: a shortform comprehensive outcome measure. I. Psychometric properties in back pain patients. J Manipulative Physiol Ther 1999;22:50310. 54. Capuano-Pucci D, Rheault W, Aukai J, Bracke M, Day R, Pastrick M. Intratester and intertester reliability of the cervical range of motion device. Arch Phys Med Rehabil 1991;72:338-40. 55. Youdas JW, Carey JR, Garrett TR. Reliability of measurements of cervical spine range of motion— comparison of three methods. Phys Ther 1991;71:98-104; discussion 105-6. 56. Dytham C. Statistics, variables and distributions. In: Dytham C. Choosing and using statistics: a biologist’s guide. Oxford: Blackwell Science; 1999. p 40. Arch Phys Med Rehabil Vol 82, July 2001
57. Mergner T, Nardi GL, Becker W, Deecke L. The role of canalneck interaction for the perception of horizontal trunk and head rotation. Exp Brain Res 1983;49:198-208. 58. Taylor JL, McCloskey DI. Proprioception in the neck. Exp Brain Res 1988;70:351-60. 59. Karnath HO, Sievering D, Fetter M. The interactive contribution of neck muscle proprioception and vestibular stimulation to subjective “straight ahead” orientation in man. Exp Brain Res 1994; 101:140-6. 60. Mergner T, Siebold C, Schweigart G, Becker W. Human perception of horizontal trunk and head rotation in space during vestibular and neck stimulation. Exp Brain Res 1991;85:389-404. 61. Kjellman GV, Skargren EI, Oberg BE. A critical analysis of randomised clinical trials on neck pain and treatment efficacy. A review of the literature. Scand J Rehabil Med 1999;31:139-52. 62. Sheather-Reid RB, Cohen ML. Psychophysical evidence for a neuropathic component of chronic neck pain. Pain 1998;75:341-7. 63. Bogduk N. The anatomy and pathophysiology of whiplash. Clin Biomech 1986;1:92-101. 64. Barnsley L, Lord S, Bogduk N. Whiplash injury. Pain 1994;58: 283-307. 65. Spitzer WO, Skovron ML, Salmi LR, Cassidy JD, Duranceau J, Suissa S, et al. Scientific monograph of the Quebec Task Force on Whiplash-Associated Disorders: redefining “whiplash” and its management. Spine 1995;20(8 Suppl):1S-73S. 66. Richmond F. The sensorium: receptors of neck muscles and joints. In: Peterson BW, Richmond FJ, editors. Control of head movement. New York: Oxford Univ Pr; 1988. p 49-62. 67. Goodwin GM, McCloskey DI, Matthews PB. Proprioceptive illusions induced by muscle vibration: contribution by muscle spindles to perception? Science 1972;175:1382-4. 68. Goodwin GM, McCloskey DI, Matthews PB. The contribution of muscle afferents to kinesthesia shown by vibration induced illusions of movement and by the effects of paralysing joint afferents. Brain 1972;95:705-48. 69. Goodwin GM, McCloskey DI, Matthews PB. The persistence of appreciable kinesthesia after paralysing joint afferents but preserving muscle afferents. Brain Res 1972;37:326-9. 70. Clark FJ, Horch KW, Bach SM, Larson GF. Contributions of cutaneous and joint receptors to static knee-position sense in man. J Neurophysiol 1979;42:877-88. 71. Cross MJ, McCloskey DI. Position sense following surgical removal of joints in man. Brain Res 1973;55:443-5. 72. Grigg P, Finerman GA, Riley LH. Joint-position sense after total hip replacement. J Bone Joint Surg Am 1973;55:1016-25. 73. Richmond FJ, Bakker GJ, Bakker DA, Stacey MJ. The innervation of tandem muscle spindles in the cat neck. J Comp Neurol 1986; 245:483-97. 74. Bakker DA, Richmond FJ. Muscle spindle complexes in muscles around upper cervical vertebrae in the cat. J Neurophysiol 1982; 48:62-74. 75. Johansson H, Sojka P. Pathophysiological mechanisms involved in genesis and spread of muscular tension in occupational muscle pain and in chronic musculoskeletal pain syndromes: a hypothesis. Med Hypotheses 1991;35:196-203. 76. Mense S, Skeppar P. Discharge behaviour of feline gammamotoneurones following induction of an artificial myositis. Pain 1991;46:201-10. 77. Johansson H, Djupsjobacka M, Sjolander P. Influences on the gamma-muscle spindle system from muscle afferents stimulated by KCl and lactic acid. Neurosci Res 1993;16:49-57. 78. Djupsjobacka M, Johansson H, Bergenheim M, Sjolander P. Influences on the gamma-muscle-spindle system from contralateral muscle afferents stimulated by KCl and lactic acid. Neurosci Res 1995;21:301-9. 79. Djupsjobacka M, Johansson H, Bergenheim M, Wenngren BI. Influences on the gamma-muscle spindle system from muscle afferents stimulated by increased intramuscular concentrations of bradykinin and 5-HT. Neurosci Res 1995;22:325-33. 80. Johansson H, Sjolander P, Sojka P. Activity in receptor afferents from the anterior cruciate ligament evokes reflex effects on fusimotor neurones. Neurosci Res (N Y) 1990;8(1):54-9.
CERVICOCEPHALIC KINESTHETIC SENSIBILITY, Rix
81. Johansson H, Sjolander P, Sojka P. A sensory role for the cruciate ligaments. Clin Orthop 1991;268:161-78. 82. Johansson H, Sjolander P, Sojka P. Receptors in the knee joint ligaments and their role in the biomechanics of the joint. Crit Rev Biomed Eng 1991;18:341-68. 83. Sjolander P, Johansson H, Sojka P, Rehnholm A. Sensory nerve endings in the cat cruciate ligaments: a morphological investigation. Neurosci Lett 1989;102:33-8. 84. Sojka P, Johansson H, Sjolander P, Lorentzon R, Djupsjobacka M. Fusimotor neurones can be reflexly influenced by activity in receptor afferents from the posterior cruciate ligament. Brain Res 1989;483:177-83. 85. Sojka P, Sjolander P, Johansson H, Djupsjobacka M. Influence from stretch-sensitive receptors in the collateral ligaments of the
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knee joint on the gamma-muscle-spindle systems of flexor and extensor muscles. Neurosci Res 1991;11:55-62. 86. Wadell I, Johansson H, Sjolander P, Sojka P, Djupsjobacka M, Niechaj A. Fusimotor reflexes influencing secondary muscle spindle afferents from flexor and extensor muscles in the hind limb of the cat. J Physiol 1991;85:223-34. 87. Morrissey MC. Reflex inhibition of thigh muscles in knee injury. Causes and treatment. Sports Med 1989;7:263-76. Suppliers a. Performance Attainment Associates, 3550 LaBore Rd, Ste 8, St Paul, MN 55110. b. Bell Image娂; Bell Sports Inc, Route 136 E, Rantoul, IL 61866. c. Minitab Inc, 3081 Enterprise Dr, State College, PA 16801-3008.
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