Development of motor system dysfunction following whiplash injury
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Pain 103 (2003) 65–73 www.elsevier.com/locate/pain Development of motor system dysfunction following whiplash injury Michele Sterling a,*, Gwendolen Jull a, Bill Vicenzino a, Justin Kenardy b, Ross Darnell c a The Whiplash Research Unit, Department of Physiotherapy, The University of Queensland, 4072 Brisbane, Australia b Department of Psychology, The University of Queensland, 4072 Brisbane, Australia c School of Health and Rehabilitation Sciences, The University of Queensland, 4072 Brisbane, Australia Received 1 July 2002; accepted 7 October 2002 Abstract Dysfunction in the motor system is a feature of persistent whiplash associated disorders. Little is known about motor dysfunction in the early stages following injury and of its progress in those persons who recover and those who develop persistent symptoms. This study measured prospectively, motor system function (cervical range of movement (ROM), joint position error (JPE) and activity of the superficial neck flexors (EMG) during a test of cranio-cervical flexion) as well as a measure of fear of re-injury (TAMPA) in 66 whiplash subjects within 1 month of injury and then 2 and 3 months post injury. Subjects were classified at 3 months post injury using scores on the neck disability index: recovered (,8), mild pain and disability (10–28) or moderate/severe pain and disability (.30). Motor system function was also measured in 20 control subjects. All whiplash groups demonstrated decreased ROM and increased EMG (compared to controls) at 1 month post injury. This deficit persisted in the group with moderate/severe symptoms but returned to within normal limits in those who had recovered or reported persistent mild pain at 3 months. Increased EMG persisted for 3 months in all whiplash groups. Only the moderate/ severe group showed greater JPE, within 1 month of injury, which remained unchanged at 3 months. TAMPA scores of the moderate/severe group were higher than those of the other two groups. The differences in TAMPA did not impact on ROM, EMG or JPE. This study identifies, for the first time, deficits in the motor system, as early as 1 month post whiplash injury, that persisted not only in those reporting moderate/ severe symptoms at 3 months but also in subjects who recovered and those with persistent mild symptoms. q 2002 International Association for the Study of Pain. Published by Elsevier Science B.V. All rights reserved. Keywords: Whiplash; Motor dysfunction; Fear of movement/re-injury 1. Introduction risk of persistent symptoms and facilitate the development of appropriate treatment strategies. The development of chronic whiplash associated disorder Motor system dysfunction is present in persons with (WAD) occurs in 12–40% of those who sustain a whiplash persistent WAD. Changes observed include reduced cervi- injury to the cervical spine and contributes substantially to cal spine movements, disturbances in cervical kinaesthesia the economic and social costs related to this condition reflected by errors in head and neck repositioning and (Barnsley et al., 1994; Eck et al., 2001). Previous research increased electromyographic (EMG) activity in neck and has indicated that those persons with persistent symptoms of shoulder girdle muscles (Heikkila and Astrom, 1996; Oster- WAD more than 3 months after injury display changes in bauer et al., 1996; Bono et al., 2000; Jull, 2000; Nederhand cervical motor system function (Heikkila and Astrom, 1996; et al., 2000; Dall’Alba et al., 2001; Dumas, 2001; Elert et Nederhand et al., 2000; Dall’Alba et al., 2001; Dumas, al., 2001). Increased EMG activity has been demonstrated 2001; Elert et al., 2001). However, little is known about during tasks of high load demand but perhaps more relevant the early stages following an injury and of the progress in to WAD, also with functional low load activities. Neder- the motor system in those who do or do not recover within 3 hand et al. (2000), using a single arm task, showed increased months of the injury. An understanding of these changes EMG activity in upper trapezius muscles both during and early on after injury may enhance identification of those at after the movement. Jull (2000) demonstrated increased activity of the superficial neck flexor muscles during a task of supported cranio-cervical flexion in subjects with persistent WAD. These changes in EMG activity have * Corresponding author. Tel.: 1 61-7-3365-4568; fax: 161-7-3365- been interpreted as reflecting altered muscle recruitment 2775. E-mail address: firstname.lastname@example.org (M. Sterling). patterns (Nederhand et al., 2000, Jull, 2000). 0304-3959/02/$30.00 q 2002 International Association for the Study of Pain. Published by Elsevier Science B.V. All rights reserved. PII: S 0304-395 9(02)00420-7
66 M. Sterling et al. / Pain 103 (2003) 65–73 Psychological factors such as beliefs about movement medical research ethics committee of the University of induced pain and re-injury may also influence motor Queensland, the Royal Australian College of General Prac- dysfunction observed in patients with persistent WAD titioners and from the ethics committee of the Royal Bris- (Nederhand et al., 2002). Fears of movement and re-injury bane Hospital. have been associated with lumbar paraspinal muscle activity in chronic low back pain (Watson et al., 1997). Similarly, 2.3. Active range of movement fear of pain (induced experimentally) can alter lumbar spine Range of active cervical movement was measured in muscle recruitment patterns albeit in asymptomatic subjects three dimensions using an electromagnetic, motion-tracking (Moseley et al., 2002). Beliefs about fear of movement and device (Fastrak, Polhemius, USA) (Trott et al., 1996; re-injury (TAMPA) are yet to be investigated in WAD. Dall’Alba et al., 2001). Output from the device was Our study addressed the lack of information on changes in converted to Euler angles to describe the motion of sensor motor system function soon after whiplash injury and the 1 (placed on the forehead) relative to sensor 2 (placed over time course of such changes in those who recover and those C7). A custom computer program was developed to allow who report persistent pain. The aims of this study were real-time viewing of the motion trace, placement of markers threefold: to investigate the differences in motor system in the data trace and storage of data. The Fastrak system has function between those who recover and those who report been used previously to investigate cervical range of move- persistent symptoms based on their status at 3 months post ments (ROM) in neck pain disorders (Dall’Alba et al., 2001) whiplash injury; to investigate the prospective longitudinal and has been shown to be accurate to within ^0.28 (Pearcy development of changes in motor system function following and Hindle, 1989). whiplash injury; to determine whether TAMPA influences any observed changes in motor function. Three aspects of 2.4. Cervical joint position error motor system function were chosen for investigation – range of cervical movement, kinaesthetic awareness and EMG Joint position error (JPE) was measured according to activity of neck flexor muscles during cranio-cervical flex- Revel et al. (1994) by using the Fastrak system and set-up ion. described for ROM. The subjects’ ability, whilst blind- folded, to relocate the head to a natural head posture was measured following active cervical left and right rotation 2. Methods and extension. 2.1. Study design 2.5. Superficial neck flexor muscle activity A prospective longitudinal design was used to study Surface EMG was used to measure the activity of the persons who sustained a whiplash injury from within 1 superficial neck flexor muscles during the cranio-cervical month of injury to 3 months post injury. They were assessed flexion test (CCFT) (Jull, 2000; Sterling et al., 2001). The at three time frames – within 1 month of injury, 2 and 3 CCFT is a progressively staged test of cranio-cervical flex- months post injury. An asymptomatic control group was ion performed in the supine lying position without resis- assessed at three parallel time frames each 1 month apart. tance. Subjects are guided to progressively increasing ranges of flexion with use of biofeedback provided by an 2.2. Subjects air filled pressure sensor positioned behind the neck which monitors the slight flattening of the cervical lordosis which Sixty-six volunteers (21 males, 45 females, mean age occurs with the test action (Mayoux-Benhamou et al., 1994; 36.27 ^ 12.69 years) reporting neck pain as a result of a Falla et al., 2002a). To ensure high fidelity feedback, the motor vehicle crash and 20 healthy asymptomatic volun- pressure sensor was calibrated at regular intervals through- teers (eight males, 12 females, mean age 40.1 ^ 13.6 out the study using a compression tension test device. Pairs years) participated in the study. The whiplash subjects of standard Ag–AgCl electrodes (Conmed, USA) were posi- were recruited through hospital accident and emergency tioned along the lower one third of the muscle bellies of both departments, primary care practices (medical and sternocleidomastoid (SCM) muscles (Falla et al., 2002b). physiotherapy) and from advertisement within radio and The EMG signals were passed through a 10 Hz high-pass print media. They were eligible if they met the Quebec filter and amplified to 20,000 units using an AMLAB data Task Force Classification of WAD II or III (Spitzer et al., acquisition system (Associated Measurements Pty Ltd, 1995). WAD IV patients were excluded. The asymptomatic Australia). control group was recruited from the general community from print media advertisement. The asymptomatic subjects 2.6. Questionnaires were included, provided they had never experienced any prior pain or trauma to the cervical spine, head or upper Self reported pain and disability was measured in all quadrant. whiplash subjects using the neck disability index (NDI) Ethical clearance for this study was granted from the (Vernon and Mior, 1991). They also completed the measure
M. Sterling et al. / Pain 103 (2003) 65–73 67 of TAMPA questionnaire as an indicator of the fear of disability (10–28 NDI) and moderate/severe pain and movement/re-injury (Kori et al., 1990). As the control disability (.30 NDI) (Vernon, 1996). subjects had never experienced neck pain it was deemed Initial analysis was performed using a repeated measures inappropriate for them to complete the questionnaires. mixed model analysis of variance (ANOVA) with a between subjects factor of group (four levels: asymptomatic, recov- 2.7. Procedure ered, mild, moderate/severe) and a within subjects factor of time (three levels: ,1 month, 2 and 3 months post injury). The following measures were undertaken at each of the Age and gender were used as covariates in this analysis. three time points. The whiplash subjects first completed the Differences between groups were analysed using a priori NDI and TAMPA questionnaires. Testing of both whiplash contrasts. Where a significant interaction occurred between and asymptomatic subjects was performed in the following group and time, post hoc tests of simple effects were sequence ROM, JPE and CCFT. The same examiner (M.S.) performed at entry into the study (,1 month) and exit performed all tests. This examiner remained blind to the from the study (3 months) to determine where these differ- subjects’ responses on the NDI and TAMPA questionnaires. ences occurred. A repeated measures mixed model ANOVA For all tests no verbal cues/feedback were given to the with a time-changing covariate of TAMPA was used to subjects about their performance. assess the effect of TAMPA on the measures of the whiplash After completion of the questionnaires, the subjects were groups. Significance was set at P , 0:01. seated, the Fastrak sensors applied and ROM was measured. Subjects were instructed to assume a comfortable position looking straight ahead, then to perform each movement 3. Results three times. They were encouraged to move at a comfortable speed, as far as possible each time and return to the start 3.1. Subject classification on NDI at 3 months post injury positioning between each repetition. The order of move- ments assessed was flexion, left lateral flexion, right lateral The NDI scores at 3 months post injury improved or flexion, left rotation, right rotation and extension. Means of remained the same compared to the initial scores (Fig. 1) the three trials for each direction of ROM were calculated and were significantly different between the three whiplash and used for analysis. groups (P , 0:01). The NDI of the recovered group was Subjects were then blindfolded and kinaesthetic testing 3 ^ 3.1 (mean ^ SD), the mild group 18.5 ^ 5.2 and the was performed. They were asked to perform the neck move- moderate/severe group 47.9 ^ 12.2. Thirty eight percent ments within comfortable limits and return as accurately as of the whiplash subjects reported recovery by 3 months possible to the starting position, which they indicated verb- post injury. Of the remaining whiplash subjects with persis- ally. This position was recorded electronically. Three trials tent symptoms at 3 months, 33% reported mild pain and of each movement direction were performed in the follow- disability and 29% moderate/severe pain and disability ing order – left rotation, right rotation and extension. Prior based on NDI scores at 3 months. Age and gender distribu- to each new movement direction, the subjects were able to tion of the four groups is illustrated in Table 1. There was an re-align their starting position to a visible target before uneven distribution of males and females and differences in being blindfolded again. JPE was calculated by using the ages between the groups approached significance mean of the absolute errors for the three trials of each move- (P ¼ 0:03). As a consequence, age and gender were ment for the primary movement direction. included as covariates in the initial analysis. The subjects were then positioned supine, EMG electro- des were applied and the CCFT was performed. Each stage 3.2. Range of movement of the test was held for 10 s. For purposes of normalisation There was a significant main effect for group (P ¼ 0:007) of EMG data, a standard head lift task was performed. This and an interaction between group and time (P ¼ 0:02) for involved the participant performing cranio-cervical flexion all movement directions except lateral flexion (P . 0:1). and just lifting the head off the plinth. This method of Due to interaction effects, group differences for flexion, normalisation of the superficial neck flexors has been used extension, left and right rotation were examined at entry previously (Sterling et al., 2001). For EMG data, the 1 s of into the study (,1 month) and exit from the study (3 maximum root mean square (RMS) values was calculated months). for each stage of the test. The maximum RMS was standar- The groups who reported mild symptoms and moderate/ dised against EMG activity in the superficial neck flexor severe symptoms at 3 months had less range of flexion, muscles during the standard head lift task. extension, left and right rotation when compared to controls 2.8. Data analysis at the entry point into the study (,1 month post injury), (P , 0:01). There was no difference between these two The whiplash subjects were classified into one of three whiplash groups for any of these movement directions at groups based on results of the NDI at 3 months post injury. entry (P . 0:49). The group who recovered showed greater The groups were recovered (,8 NDI), mild pain and range of extension than the other two whiplash groups
68 M. Sterling et al. / Pain 103 (2003) 65–73 Fig. 1. Initial (1 month) and final (3 months) classification of whiplash subjects based on NDI scores. Mild pain and disability (10–28 NDI), moderate/severe pain and disability (.30 NDI) and recovered (,8 NDI). (P , 0:005) at entry but less than that of the control group (marginal mean ^ SEM) compared to all other groups (P , 0:01). Range of movement of the groups who recov- (P , 0:01). There were no between group differences in ered or reported mild symptoms improved with time. At 3 those who recovered (3.6 ^ 0.58), those with persistent months post injury, their movement (in all directions) was mild symptoms (2.7 ^ 0.48) and the control group no longer different from controls (P . 0:3). In contrast, the (2.8 ^ 0.58) (P . 0:1). There was no effect of age or gender movement loss at entry persisted in the group with moder- on JPE (P . 0:06) (Table 2). ate/severe symptoms and remained less than that of the control group at 3 months – the final assessment point 3.4. EMG activity of superficial neck flexors (P , 0:01). The marginal means (^SEM) of the four There was no interaction effect between group and time groups for the movements of flexion, extension, left and for the EMG activity measured during the stages of the right rotation are presented in Figs. 2 and 3. The effect of CCFT. Analysis of the main effects revealed a significant age on range of movement was significant only for exten- difference in EMG activity between the groups sion, left and right rotation (P , 0:01), with ROM decreas- (P , 0:0001) and this difference persisted over time (Fig. ing with increasing age. There was no effect of gender on 5). EMG activity of the superficial neck flexors in the group any measure of ROM (P . 0:2). with moderate/severe symptoms was 40 ^ 4% (estimated mean ^ SEM), which was significantly greater than the 3.3. JPE EMG activity recorded for all other groups (P , 0:01). EMG activity of the groups who recovered (29 ^ 4%) or The results of data for JPE are presented in Fig. 4. There had mild symptoms at 3 months (27 ^ 3%) was also signif- was no interaction effect between group and time for all icantly greater than that of the control group (16 ^ 3%) three measures of JPE, indicating that there was no change (P , 0:01). There was no effect of age or gender on EMG over time in any JPE direction. When the main effects were (P . 0:2). considered, there was a significant difference between the groups for JPE (right rotation) (P ¼ 0:002) but no group 3.5. TAMPA difference for JPE (left rotation, extension) (P . 0:3). The group with persistent moderate/severe symptoms had a There was a significant difference between the three significantly greater JPE (right rotation) of 4.8 ^ 0.48 whiplash groups for the TAMPA score (P ¼ 0:0001). As Table 1 The age, gender and classification of subject groups at 3 months according to the NDI scores (Vernon, 1996) Group Number Age (years) (mean ^ SD) Gender % female NDI classification NDI (mean ^ SD) Recovered group 25 33.5 ^ 10.2 60 ,8 3.0 ^ 3.1 Mild pain and disability group 22 34.7 ^ 12.6 64 10–28 18.5 ^ 5.2 Moderate/severe pain and 19 41.3 ^ 13.6 84 . 30 47.9 ^ 12.2 disability group Control group 20 40.1 ^ 13.6 60 – –
M. Sterling et al. / Pain 103 (2003) 65–73 69 percent of our cohort, of volunteers sustaining a whiplash injury, reported ongoing pain at 3 months post injury, a similar figure to data from previous longitudinal studies (Radanov et al., 1995; Mayou and Bryant, 1996; Gargan et al., 1997). Twenty-nine percent of the cohort reported persistent moderate or severe symptoms. Values obtained for control subjects for all measures of motor function were similar to those previously reported (Revel, 1991; Jull, 2000; Dall’Alba et al., 2001). Deficits in cervical ROM were present within 1 month of injury in all whiplash subjects. The loss in ROM persisted in the group who reported moderate/severe symptoms at 3 months, while movement in the groups who reported mild symptoms or who had recovered at 3 months improved with time and returned to ranges that were no longer different from healthy controls. Most cross-sectional studies investi- gating ROM in chronic WAD have demonstrated decreased cervical movement (Osterbauer et al., 1996; Bono et al., 2000; Dall’Alba et al., 2001; Dumas, 2001). However, a recent longitudinal study suggested that although ROM was decreased in the first few weeks after injury, by 3 Fig. 2. Means and standard errors of the mean (SEM) for all groups (control, months this loss was regained (Kasch et al., 2001) which recovered, mild pain and moderate/severe pain) over time (1, 2 and 3 seems at odds with our findings. However, Kasch et al. months post injury) for active range of extension and flexion. (2001) did not attempt to differentiate between recovered and non-recovered subjects as we did. The findings of our can be seen from the mean values in Fig. 6, the group with study reinforce the need to not only differentiate between persistent moderate/severe symptoms had significantly recovered and non-recovered subjects but also between higher TAMPA scores than the other two groups (marginal those who continue to report higher levels of pain and mean 40.55 ^ 2). In the groups who recovered or reported disability from those with mild symptoms. mild symptoms at 3 months, the TAMPA scores improved significantly over time (P , 0:05) whereas there was no change over time in the scores of the moderate/severe group (P ¼ 0:783). When TAMPA scores were included in the analysis of the three whiplash groups, group differences remained signifi- cant for JPE (right rotation) (P ¼ 0:01) and EMG (P , 0:01). With respect to ROM, group differences at the time points described above also remained significant (P , 0:01). There was no interaction between group and TAMPA for any measure of motor function (P . 0:13) suggesting that the effect of TAMPA on the motor measures is similar irrespective of group allocation. The effect size for TAMPA on the measures of motor activity was small (partial eta squared ranged from 0.00006 to 0.02). 4. Discussion The results of this study provide the first evidence of early changes in motor system function following whiplash injury. These changes were apparent within 1 month of injury and occurred not only in those reporting moderate/ severe symptoms at 3 months but also in subjects who recovered and those with persistent mild symptoms. In all Fig. 3. Means and standard errors of the mean (SEM) for all groups (control, whiplash groups certain specific changes in motor system recovered, mild pain and moderate/severe pain) over time (1, 2 and 3 function persisted over the 3 month study period. Sixty-two months post injury) for active range of left and right rotation.
70 M. Sterling et al. / Pain 103 (2003) 65–73 Fig. 4. Means and standard errors of the mean (SEM) for all groups (control, recovered, mild pain and moderate/severe pain) over time (1, 2 and 3 months post injury) for joint position error (JPE) from right rotation. Evidence of altered kinaesthetic awareness as measured during the CCFT is thought to be indicative of alterations in using JPE was apparent only in the group of whiplash patterns of muscle activation and recruitment and has been subjects reporting persistent moderate/severe pain at 3 identified in patients with chronic neck pain of both trau- months. This occurred in one movement direction – reloca- matic and non-traumatic origin (Jull, 2000; Jull et al., 2002). tion from right rotation, was present within 1 month of This study demonstrates that these changes occur soon after injury and showed no change over time. These results injury and persist not only in those reporting ongoing symp- support our previous research where chronic WAD subjects toms at 3 months post injury but also in those whose symp- with a higher neck disability index (in this case the North- toms have resolved during this time. Research into low back wick Park questionnaire) demonstrated greater JPE (Trelea- pain has shown that altered muscle recruitment persists ven et al., 2002). Whilst only relocation from right rotation despite the patient reporting recovery and may be one factor was affected in this current study, previous researchers have involved in high rate of symptom recurrence in this condi- noted errors in chronic WAD subjects in other movement tion (Hides et al., 2001). Whether the whiplash patients who directions including extension, flexion and left rotation recovered in this study continue to demonstrate increased (Heikkila and Astrom, 1996; Treleaven et al., 2002) muscle activity past the 3 month period and whether this although Treleaven et al. (2002) showed greater JPE with group reports recurrence of pain at some later date is right rotation. The reasons for this discrepancy are unclear. presently under investigation. The majority of subjects (16 of 19) in the moderate/severe The contribution of physical and psychosocial factors to group reported bilateral neck pain discounting the possibi- the development of chronic symptoms has been studied lity that the side of pain is responsible for this finding. Hand extensively in chronic low back pain (Fritz et al., 2001), dominance was not considered in this study and could be but very little attention has been paid to their role in cervical associated with this finding. Additionally, the subjects in spine pain. Whilst the moderate/severe group in this study this study were only 3 months post injury as opposed to showed elevated scores on the TAMPA scale – similar to the above-mentioned studies using chronic WAD subjects those seen in chronic low back pain (Crombez et al., 1999), with longer symptom duration. Whether JPE in other direc- differences in motor function between the whiplash groups tions emerge in time remains to be seen and may require remained significant when TAMPA scores were taken into further investigation. account. Furthermore the relationship between TAMPA and Increased activity in the superficial neck flexor muscles the measures of motor function was weak. This would Table 2 Marginal means (SEM) of joint position error (JPE) right and left rotation and extension for all groups a Group JPE (right rotation) JPE (left rotation) JPE (extension) (mean ^ SEM) (mean ^ SEM) (mean ^ SEM) Recovered 3.6 ^ 0.3 3.0 ^ 0.2 3.3 ^ 0.3 Mild pain and disability 2.7 ^ 0.3 2.7 ^ 0.2 3.4 ^ 0.3 Moderate/severe pain and disability 4.8 ^ 0.3 3.2 ^ 0.3 4.1 ^ 0.3 Controls 2.7 ^ 0.3 2.6 ^ 0.3 2.8 ^ 0.3 a Values in bold are significantly greater than control for P , 0:01.
M. Sterling et al. / Pain 103 (2003) 65–73 71 Fig. 5. Normalised EMG (mean and SEM) of the superficial neck flexors for all groups (control, recovered, mild pain and moderate/severe pain) over time (1,2 and 3 months post injury) during the CCFT. suggest that ROM loss, increased superficial neck flexor recruitment patterns and effects on supraspinal neurons muscle activity during the CCFT and JPE occurred indepen- (Woolf and Wall, 1986; Mense and Skeppar, 1991; Made- dently of fear of movement/re-injury. The finding that leine et al., 1999; Andersen et al., 2000; Ro and Capra, increased muscle activity occurred in the WAD subjects 2001; Thurnberg et al., 2001). Most of these studies have even when controlled for TAMPA beliefs occur is contrary used animal models or induced experimental muscle pain as to findings in chronic low back pain where abnormal para- a model for acute pain making it difficult to extrapolate the spinal muscle activity has shown to be influenced by findings to the clinical situation. Furthermore little is known psychological factors (Watson et al., 1997). Our findings about the long-term nature of such changes. Nevertheless indicate that motor system changes in this population are evidence from clinical studies of chronic pain would suggest not totally explained by the subjects’ TAMPA, confirming that certain motor system changes do persist (Hodges and suggestions that the relationship between fear-avoidance Richardson, 1999; Madeleine et al., 1999). The findings of beliefs and disability in cervical pain may be weaker than this study may reflect underlying disturbances in motor that for lumbar pain (George et al., 2001). function as a consequence of the initial peripheral nocicep- Experimental investigations have provided evidence that tive input (for example from injured cervical structures acute musculoskeletal pain is capable of inducing changes following whiplash injury) in the acute stage of injury, in motor system function such as alteration of spinal motor which appear to persist over time. Further investigation of reflexes, effects on the gamma motor system, altered motor such potential mechanisms in WAD is required. Fig. 6. Means and standard errors of the mean (SEM) for three whiplash groups (recovered, mild pain and moderate/severe pain) over time (1,2 and 3 months post injury) for scores of TAMPA questionnaire.
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