Development of motor system dysfunction following whiplash injury

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1 Pain 103 (2003) 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 The development of chronic whiplash associated disorder (WAD) occurs in 12 40% of those who sustain a whiplash injury to the cervical spine and contributes substantially to the economic and social costs related to this condition (Barnsley et al., 1994; Eck et al., 2001). Previous research has indicated that those persons with persistent symptoms of WAD more than 3 months after injury display changes in cervical motor system function (Heikkila and Astrom, 1996; Nederhand et al., 2000; Dall Alba et al., 2001; Dumas, 2001; Elert et al., 2001). However, little is known about the early stages following an injury and of the progress in the motor system in those who do or do not recover within 3 months of the injury. An understanding of these changes early on after injury may enhance identification of those at * Corresponding author. Tel.: ; fax: address: m.sterling@shrs.uq.edu.au (M. Sterling). risk of persistent symptoms and facilitate the development of appropriate treatment strategies. Motor system dysfunction is present in persons with persistent WAD. Changes observed include reduced cervical spine movements, disturbances in cervical kinaesthesia reflected by errors in head and neck repositioning and increased electromyographic (EMG) activity in neck and shoulder girdle muscles (Heikkila and Astrom, 1996; Osterbauer et al., 1996; Bono et al., 2000; Jull, 2000; Nederhand et al., 2000; Dall Alba et al., 2001; Dumas, 2001; Elert et al., 2001). Increased EMG activity has been demonstrated during tasks of high load demand but perhaps more relevant to WAD, also with functional low load activities. Nederhand et al. (2000), using a single arm task, showed increased EMG activity in upper trapezius muscles both during and 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 been interpreted as reflecting altered muscle recruitment patterns (Nederhand et al., 2000, Jull, 2000) /02/$30.00 q 2002 International Association for the Study of Pain. Published by Elsevier Science B.V. All rights reserved. PII: S (02)

2 66 M. Sterling et al. / Pain 103 (2003) Psychological factors such as beliefs about movement induced pain and re-injury may also influence motor dysfunction observed in patients with persistent WAD (Nederhand et al., 2002). Fears of movement and re-injury have been associated with lumbar paraspinal muscle activity in chronic low back pain (Watson et al., 1997). Similarly, fear of pain (induced experimentally) can alter lumbar spine muscle recruitment patterns albeit in asymptomatic subjects (Moseley et al., 2002). Beliefs about fear of movement and re-injury (TAMPA) are yet to be investigated in WAD. Our study addressed the lack of information on changes in motor system function soon after whiplash injury and the time course of such changes in those who recover and those who report persistent pain. The aims of this study were threefold: to investigate the differences in motor system function between those who recover and those who report persistent symptoms based on their status at 3 months post whiplash injury; to investigate the prospective longitudinal development of changes in motor system function following whiplash injury; to determine whether TAMPA influences any observed changes in motor function. Three aspects of motor system function were chosen for investigation range of cervical movement, kinaesthetic awareness and EMG activity of neck flexor muscles during cranio-cervical flexion. 2. Methods 2.1. Study design A prospective longitudinal design was used to study persons who sustained a whiplash injury from within 1 month of injury to 3 months post injury. They were assessed at three time frames within 1 month of injury, 2 and 3 months post injury. An asymptomatic control group was assessed at three parallel time frames each 1 month apart Subjects Sixty-six volunteers (21 males, 45 females, mean age ^ years) reporting neck pain as a result of a motor vehicle crash and 20 healthy asymptomatic volunteers (eight males, 12 females, mean age 40.1 ^ 13.6 years) participated in the study. The whiplash subjects were recruited through hospital accident and emergency departments, primary care practices (medical and physiotherapy) and from advertisement within radio and print media. They were eligible if they met the Quebec Task Force Classification of WAD II or III (Spitzer et al., 1995). WAD IV patients were excluded. The asymptomatic control group was recruited from the general community from print media advertisement. The asymptomatic subjects were included, provided they had never experienced any prior pain or trauma to the cervical spine, head or upper quadrant. Ethical clearance for this study was granted from the medical research ethics committee of the University of Queensland, the Royal Australian College of General Practitioners and from the ethics committee of the Royal Brisbane Hospital Active range of movement Range of active cervical movement was measured in three dimensions using an electromagnetic, motion-tracking device (Fastrak, Polhemius, USA) (Trott et al., 1996; Dall Alba et al., 2001). Output from the device was converted to Euler angles to describe the motion of sensor 1 (placed on the forehead) relative to sensor 2 (placed over C7). A custom computer program was developed to allow real-time viewing of the motion trace, placement of markers in the data trace and storage of data. The Fastrak system has been used previously to investigate cervical range of movements (ROM) in neck pain disorders (Dall Alba et al., 2001) and has been shown to be accurate to within ^0.28 (Pearcy and Hindle, 1989) Cervical joint position error Joint position error (JPE) was measured according to Revel et al. (1994) by using the Fastrak system and set-up described for ROM. The subjects ability, whilst blindfolded, to relocate the head to a natural head posture was measured following active cervical left and right rotation and extension Superficial neck flexor muscle activity Surface EMG was used to measure the activity of the superficial neck flexor muscles during the cranio-cervical flexion test (CCFT) (Jull, 2000; Sterling et al., 2001). The CCFT is a progressively staged test of cranio-cervical flexion performed in the supine lying position without resistance. Subjects are guided to progressively increasing ranges of flexion with use of biofeedback provided by an air filled pressure sensor positioned behind the neck which monitors the slight flattening of the cervical lordosis which occurs with the test action (Mayoux-Benhamou et al., 1994; Falla et al., 2002a). To ensure high fidelity feedback, the pressure sensor was calibrated at regular intervals throughout the study using a compression tension test device. Pairs of standard Ag AgCl electrodes (Conmed, USA) were positioned along the lower one third of the muscle bellies of both sternocleidomastoid (SCM) muscles (Falla et al., 2002b). The EMG signals were passed through a 10 Hz high-pass filter and amplified to 20,000 units using an AMLAB data acquisition system (Associated Measurements Pty Ltd, Australia) Questionnaires Self reported pain and disability was measured in all whiplash subjects using the neck disability index (NDI) (Vernon and Mior, 1991). They also completed the measure

3 M. Sterling et al. / Pain 103 (2003) of TAMPA questionnaire as an indicator of the fear of movement/re-injury (Kori et al., 1990). As the control subjects had never experienced neck pain it was deemed inappropriate for them to complete the questionnaires Procedure The following measures were undertaken at each of the three time points. The whiplash subjects first completed the NDI and TAMPA questionnaires. Testing of both whiplash and asymptomatic subjects was performed in the following sequence ROM, JPE and CCFT. The same examiner (M.S.) performed all tests. This examiner remained blind to the subjects responses on the NDI and TAMPA questionnaires. For all tests no verbal cues/feedback were given to the subjects about their performance. After completion of the questionnaires, the subjects were 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 three times. They were encouraged to move at a comfortable speed, as far as possible each time and return to the start positioning between each repetition. The order of movements assessed was flexion, left lateral flexion, right lateral flexion, left rotation, right rotation and extension. Means of the three trials for each direction of ROM were calculated and used for analysis. Subjects were then blindfolded and kinaesthetic testing was performed. They were asked to perform the neck movements within comfortable limits and return as accurately as possible to the starting position, which they indicated verbally. This position was recorded electronically. Three trials of each movement direction were performed in the following order left rotation, right rotation and extension. Prior to each new movement direction, the subjects were able to re-align their starting position to a visible target before being blindfolded again. JPE was calculated by using the mean of the absolute errors for the three trials of each movement for the primary movement direction. The subjects were then positioned supine, EMG electrodes were applied and the CCFT was performed. Each stage of the test was held for 10 s. For purposes of normalisation of EMG data, a standard head lift task was performed. This involved the participant performing cranio-cervical flexion and just lifting the head off the plinth. This method of normalisation of the superficial neck flexors has been used previously (Sterling et al., 2001). For EMG data, the 1 s of maximum root mean square (RMS) values was calculated for each stage of the test. The maximum RMS was standardised against EMG activity in the superficial neck flexor muscles during the standard head lift task Data analysis The whiplash subjects were classified into one of three groups based on results of the NDI at 3 months post injury. The groups were recovered (,8 NDI), mild pain and disability (10 28 NDI) and moderate/severe pain and disability (.30 NDI) (Vernon, 1996). Initial analysis was performed using a repeated measures mixed model analysis of variance (ANOVA) with a between subjects factor of group (four levels: asymptomatic, recovered, mild, moderate/severe) and a within subjects factor of time (three levels:,1 month, 2 and 3 months post injury). Age and gender were used as covariates in this analysis. Differences between groups were analysed using a priori contrasts. Where a significant interaction occurred between group and time, post hoc tests of simple effects were performed at entry into the study (,1 month) and exit from the study (3 months) to determine where these differences occurred. A repeated measures mixed model ANOVA with a time-changing covariate of TAMPA was used to assess the effect of TAMPA on the measures of the whiplash groups. Significance was set at P, 0: Results 3.1. Subject classification on NDI at 3 months post injury The NDI scores at 3 months post injury improved or remained the same compared to the initial scores (Fig. 1) and were significantly different between the three whiplash groups (P, 0:01). The NDI of the recovered group was 3 ^ 3.1 (mean ^ SD), the mild group 18.5 ^ 5.2 and the moderate/severe group 47.9 ^ Thirty eight percent of the whiplash subjects reported recovery by 3 months post injury. Of the remaining whiplash subjects with persistent symptoms at 3 months, 33% reported mild pain and disability and 29% moderate/severe pain and disability based on NDI scores at 3 months. Age and gender distribution of the four groups is illustrated in Table 1. There was an uneven distribution of males and females and differences in ages between the groups approached significance (P ¼ 0:03). As a consequence, age and gender were included as covariates in the initial analysis Range of movement There was a significant main effect for group (P ¼ 0:007) and an interaction between group and time (P ¼ 0:02) for all movement directions except lateral flexion (P. 0:1). Due to interaction effects, group differences for flexion, extension, left and right rotation were examined at entry into the study (,1 month) and exit from the study (3 months). The groups who reported mild symptoms and moderate/ severe symptoms at 3 months had less range of flexion, extension, left and right rotation when compared to controls at the entry point into the study (,1 month post injury), (P, 0:01). There was no difference between these two whiplash groups for any of these movement directions at entry (P. 0:49). The group who recovered showed greater range of extension than the other two whiplash groups

4 68 M. Sterling et al. / Pain 103 (2003) 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 (P, 0:01). Range of movement of the groups who recovered or reported mild symptoms improved with time. At 3 months post injury, their movement (in all directions) was no longer different from controls (P. 0:3). In contrast, the movement loss at entry persisted in the group with moderate/severe symptoms and remained less than that of the control group at 3 months the final assessment point (P, 0:01). The marginal means (^SEM) of the four groups for the movements of flexion, extension, left and right rotation are presented in Figs. 2 and 3. The effect of age on range of movement was significant only for extension, left and right rotation (P, 0:01), with ROM decreasing with increasing age. There was no effect of gender on any measure of ROM (P. 0:2) JPE The results of data for JPE are presented in Fig. 4. There was no interaction effect between group and time for all three measures of JPE, indicating that there was no change over time in any JPE direction. When the main effects were considered, there was a significant difference between the groups for JPE (right rotation) (P ¼ 0:002) but no group difference for JPE (left rotation, extension) (P. 0:3). The group with persistent moderate/severe symptoms had a significantly greater JPE (right rotation) of 4.8 ^ 0.48 (marginal mean ^ SEM) compared to all other groups (P, 0:01). There were no between group differences in those who recovered (3.6 ^ 0.58), those with persistent mild symptoms (2.7 ^ 0.48) and the control group (2.8 ^ 0.58)(P. 0:1). There was no effect of age or gender on JPE (P. 0:06) (Table 2) EMG activity of superficial neck flexors There was no interaction effect between group and time for the EMG activity measured during the stages of the CCFT. Analysis of the main effects revealed a significant difference in EMG activity between the groups (P, 0:0001) and this difference persisted over time (Fig. 5). EMG activity of the superficial neck flexors in the group with moderate/severe symptoms was 40 ^ 4% (estimated mean ^ SEM), which was significantly greater than the EMG activity recorded for all other groups (P, 0:01). EMG activity of the groups who recovered (29 ^ 4%) or had mild symptoms at 3 months (27 ^ 3%) was also significantly greater than that of the control group (16 ^ 3%) (P, 0:01). There was no effect of age or gender on EMG (P. 0:2) TAMPA There was a significant difference between the three 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 ^ , ^ 3.1 Mild pain and disability group ^ ^ 5.2 Moderate/severe pain and ^ ^ 12.2 disability group Control group ^

5 M. Sterling et al. / Pain 103 (2003) Fig. 2. 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 active range of extension and flexion. can be seen from the mean values in Fig. 6, the group with persistent moderate/severe symptoms had significantly higher TAMPA scores than the other two groups (marginal mean ^ 2). In the groups who recovered or reported 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 significant 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 to 0.02). 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 investigating 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 months this loss was regained (Kasch et al., 2001) which seems at odds with our findings. However, Kasch et al. (2001) did not attempt to differentiate between recovered and non-recovered subjects as we did. The findings of our study reinforce the need to not only differentiate between recovered and non-recovered subjects but also between those who continue to report higher levels of pain and disability from those with mild symptoms. 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 whiplash groups certain specific changes in motor system function persisted over the 3 month study period. Sixty-two Fig. 3. 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 active range of left and right rotation.

6 70 M. Sterling et al. / Pain 103 (2003) 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 using JPE was apparent only in the group of whiplash subjects reporting persistent moderate/severe pain at 3 months. This occurred in one movement direction relocation from right rotation, was present within 1 month of injury and showed no change over time. These results support our previous research where chronic WAD subjects with a higher neck disability index (in this case the Northwick Park questionnaire) demonstrated greater JPE (Treleaven et al., 2002). Whilst only relocation from right rotation was affected in this current study, previous researchers have noted errors in chronic WAD subjects in other movement directions including extension, flexion and left rotation (Heikkila and Astrom, 1996; Treleaven et al., 2002) although Treleaven et al. (2002) showed greater JPE with right rotation. The reasons for this discrepancy are unclear. The majority of subjects (16 of 19) in the moderate/severe group reported bilateral neck pain discounting the possibility that the side of pain is responsible for this finding. Hand dominance was not considered in this study and could be associated with this finding. Additionally, the subjects in this study were only 3 months post injury as opposed to the above-mentioned studies using chronic WAD subjects with longer symptom duration. Whether JPE in other directions emerge in time remains to be seen and may require further investigation. Increased activity in the superficial neck flexor muscles during the CCFT is thought to be indicative of alterations in patterns of muscle activation and recruitment and has been identified in patients with chronic neck pain of both traumatic and non-traumatic origin (Jull, 2000; Jull et al., 2002). This study demonstrates that these changes occur soon after injury and persist not only in those reporting ongoing symptoms at 3 months post injury but also in those whose symptoms have resolved during this time. Research into low back pain has shown that altered muscle recruitment persists despite the patient reporting recovery and may be one factor involved in high rate of symptom recurrence in this condition (Hides et al., 2001). Whether the whiplash patients who recovered in this study continue to demonstrate increased muscle activity past the 3 month period and whether this group reports recurrence of pain at some later date is presently under investigation. The contribution of physical and psychosocial factors to the development of chronic symptoms has been studied extensively in chronic low back pain (Fritz et al., 2001), but very little attention has been paid to their role in cervical spine pain. Whilst the moderate/severe group in this study showed elevated scores on the TAMPA scale similar to those seen in chronic low back pain (Crombez et al., 1999), differences in motor function between the whiplash groups remained significant when TAMPA scores were taken into account. Furthermore the relationship between TAMPA and 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) (mean ^ SEM) JPE (left rotation) (mean ^ SEM) JPE (extension) (mean ^ SEM) Recovered 3.6 ^ ^ ^ 0.3 Mild pain and disability 2.7 ^ ^ ^ 0.3 Moderate/severe pain and disability 4.8 ^ ^ ^ 0.3 Controls 2.7 ^ ^ ^ 0.3 a Values in bold are significantly greater than control for P, 0:01.

7 M. Sterling et al. / Pain 103 (2003) 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 muscle activity during the CCFT and JPE occurred independently of fear of movement/re-injury. The finding that increased muscle activity occurred in the WAD subjects even when controlled for TAMPA beliefs occur is contrary to findings in chronic low back pain where abnormal paraspinal muscle activity has shown to be influenced by psychological factors (Watson et al., 1997). Our findings indicate that motor system changes in this population are not totally explained by the subjects TAMPA, confirming suggestions that the relationship between fear-avoidance beliefs and disability in cervical pain may be weaker than that for lumbar pain (George et al., 2001). Experimental investigations have provided evidence that acute musculoskeletal pain is capable of inducing changes in motor system function such as alteration of spinal motor reflexes, effects on the gamma motor system, altered motor recruitment patterns and effects on supraspinal neurons (Woolf and Wall, 1986; Mense and Skeppar, 1991; Madeleine et al., 1999; Andersen et al., 2000; Ro and Capra, 2001; Thurnberg et al., 2001). Most of these studies have used animal models or induced experimental muscle pain as a model for acute pain making it difficult to extrapolate the findings to the clinical situation. Furthermore little is known about the long-term nature of such changes. Nevertheless evidence from clinical studies of chronic pain would suggest that certain motor system changes do persist (Hodges and Richardson, 1999; Madeleine et al., 1999). The findings of this study may reflect underlying disturbances in motor function as a consequence of the initial peripheral nociceptive input (for example from injured cervical structures following whiplash injury) in the acute stage of injury, which appear to persist over time. Further investigation of 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.

8 72 M. Sterling et al. / Pain 103 (2003) The results of this study may have implications for the clinical management of whiplash-injured patients. Randomised controlled trials of specific retraining of the craniocervical flexion movement and rehabilitation of cervical kinaesthesia have demonstrated efficacy in the treatment of chronic neck pain syndromes albeit mainly neck pain of a non-traumatic cause (Revel et al., 1994; Jull et al., 2002). In view of the findings of this study, where similar motor deficits were shown to occur within 1 month of injury, the inclusion of such rehabilitation programs may be beneficial in the management of acute WAD. Acknowledgements This study was supported by Suncorp Metway Insurance, Queensland and Centre of National Research on Disability and Rehabilitation Medicine (CONROD). References Andersen O, Graven-Nielsen T, Matre D, Arendt-Nielsen L. 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