Bilateral Sensorimotor Abnormalities in Unilateral Lateral Epicondylalgia

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1 490 ORIGINAL ARTICLE Bilateral Sensorimotor Abnormalities in Unilateral Lateral Epicondylalgia Leanne M. Bisset, MPhty, Trevor Russell, PhD, Stephen Bradley, MPhty, Bernadette Ha, MPhty, Bill T. Vicenzino, PhD ABSTRACT. Bisset LM, Russell T, Bradley S, Ha B, Vicenzino BT. Bilateral sensorimotor abnormalities in unilateral lateral epicondylalgia. Arch Phys Med Rehabil 2006;87: Objective: To evaluate impairments in motor function of the upper limb in unilateral lateral epicondylalgia. Design: Assessor-blinded, case-controlled study. Setting: University laboratory. Participants: Forty participants with lateral epicondylalgia and 40 age- and sex-matched controls were recruited from the general community. Interventions: Not applicable. Main Outcome Measures: Wrist posture adopted during a grip test, grip strength force, as well as upper-limb reaction times and speed of movement. Results: Participants with unilateral lateral epicondylalgia adopted wrist postures that were on average 11 less extended, bilaterally, than controls (P.000). This was paralleled by increased upper-limb reaction times and reduced speed of movement (mean differences, 2% 15%) in both affected and unaffected limbs. Pain-free grip strength was reduced on the involved side (mean difference, 170N; 95% confidence interval, N). Conclusions: Motor deficits may be modifiable through exercise and postural retraining. Although further work is required to evaluate the clinical efficacy of such an approach, health care practitioners have an emerging evidence base on which to base their management of lateral epicondylalgia. Key Words: Hand; Rehabilitation; Tennis elbow; Wrist by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation LATERAL EPICONDYLALGIA, also known as tennis elbow, is a condition of pain experienced over the lateral humeral epicondyle, which is associated with gripping or manipulative activities of the hand. Its prevalence has been reported at 3% in the general population, 1 up to 15% in certain repetitive hand task occupations, 2-4 and as high as 50% in tennis players. 5-8 This condition substantially impacts on participation at work with absenteeism being as high as 12 weeks in as many as 30% of those afflicted. 9 From the Division of Physiotherapy, School of Health and Rehabilitation Sciences, University of Queensland, Australia. Supported by the National Health and Medical Research Council, Australia (grant no ). 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 authors or upon any organization with which the authors are associated. Reprint requests to Bill T. Vicenzino, PhD, Division of Physiotherapy, School of Health and Rehabilitation Sciences, University of Queensland, St Lucia, QLD 4072, Australia, b.vicenzino@uq.edu.au /06/ $32.00/0 doi: /j.apmr There exists a growing body of knowledge that is challenging original theories on the etiology of lateral epicondylalgia. Current evidence suggests that lateral epicondylalgia is characterized by structural changes to the extensor carpi radialis brevis tendon with neovascularization, disruption of collagen, and mucoid degeneration without inflammation, along with significantly higher levels of glutamate (an excitatory amino acid) but not prostaglandin E There is mounting evidence that lateral epicondylalgia does not involve an inflammatory response, but rather impaired nociceptive system function associated with degenerative tissue changes ,14-16 In addition to pain, patients with lateral epicondylalgia exhibit an impaired ability to perform tasks that require gripping, with reduced grip force and deficits in wrist extensor isokinetic strength Pienimaki et al 21 compared motor performance in participants with lateral epicondylalgia to age- and sexmatched controls and reported increased reaction times and reduced speed of movement in the upper limb. Also noteworthy is an earlier study 22 of the tennis backhand stroke in players with lateral epicondylalgia. Kelley et al 22 identified marked dysfunction of forearm muscle activation, especially of the extensor carpi radialis muscles, along with qualitatively determined altered kinematics of the upper limb when compared with healthy controls. We have also noted in clinic that patients with lateral epicondylalgia tend to spontaneously adopt a relatively flexed-wrist posture during grip strength testing, which is not an optimal wrist posture for maximal force output Thus, evidence is mounting for a model of lateral epicondylalgia that incorporates impairment of the motor system, dysfunction of the nociceptive system and altered local collagen structure in lateral epicondylalgia. 26 The aim of the current study was to evaluate motor impairments in participants with lateral epicondylalgia by measuring wrist posture adopted during gripping and to determine reaction time and speed of movement of the upper limb in patients with lateral epicondylalgia. METHODS An assessor-blinded, case controlled study was conducted to compare motor performance in lateral epicondylalgia participants compared with age- and sex-matched controls. Participants Forty participants reporting unilateral lateral epicondylalgia were recruited for this study. Participants were included in the study if they experienced unilateral pain over the lateral epicondyle of at least 6 weeks in duration that was aggravated by palpation, gripping, and resisted wrist and/or finger extension. 27 Forty age- and sex-matched participants who had no history of lateral epicondylalgia served as the control group. Participants were excluded from the study if they had experienced neck or arm pain (other than lateral epicondylalgia for the lateral epicondylalgia group) which had required treatment or prevented them from participating in their usual work or recreational activities. Participants were also excluded if they

2 SENSORIMOTOR ABNORMALITIES IN EPICONDYLALGIA, Bisset 491 had any other concomitant bony, neurologic, or systemic disease or had had any treatment (apart from oral or topical medications) in the previous 6 months. All participants were recruited from the general community through media advertising. Characteristics of the study participants are shown in table 1. Ethics approval was granted by the institutional review board and informed written consent was obtained from all participants. Measures Motor performance was measured in a number of ways: (1) measures of spontaneous wrist posture in the sagittal plane adopted during a grip task; (2) grip strength with and without pain; and (3) upper-limb reaction times and speed of movement. Table 1: Descriptive Statistics for the Lateral Epicondylalgia (n 40) and Control Groups (n 40) Fig 1. Identifying markers were placed on the participant s lateral epicondyle, lateral ulnar styloid process, and the lateral base of the fifth metacarpal. Relative wrist angle (in degrees) in the sagittal plane during a gripping task was measured using a digital image and specialized software. Wrist Posture and Grip Strength To measure wrist posture, we placed markers on the skin overlying the lateral epicondyle, lateral ulnar styloid process, and the lateral surface of the head of the fifth metacarpal (fig 1). Each participant was positioned in standing with the upper limb to be measured in 90 shoulder flexion, full elbow extension, and forearm pronation. We asked the participant to minimize shoulder rotation but gave no advice regarding the wrist position. The lens of the digital camera was positioned level with and at a set distance of 100cm from the wrist. A digital grip dynamometer a was placed in the participant s hand and a measure of pain-free grip strength was taken. It has been previously reported that pain-free grip strength is more sensitive than maximum grip strength in detecting the level of severity in lateral epicondylalgia. 19 For the measure of painfree grip strength, the participant was informed to stop squeezing the dynamometer when their pain was first provoked. 28 A digital photograph was taken of the upper limb during the pain-free grip test and the process was repeated 3 times with an intervening 30-second rest interval. This process was then repeated for the opposite unaffected side. The unaffected side of the lateral epicondylalgia group and the control group all gripped the dynamometer maximally because they were pain free. Maximal grip strength on the affected side in the lateral epicondylalgia group was measured last, and the participant was asked to squeeze the dynamometer to their highest tolerable level of pain. This test was also performed 3 times with 30-second rest intervals. The digital images were downloaded onto a desktop computer and a measure of wrist angle in the sagittal plane was obtained using a validated software program. 29,b A relative reference point of 0 was given by the line extending through the lateral epicondyle and lateral ulnar styloid. All measures of wrist angle were documented in relation to this point, with positive values for extension and negative values for flexion. Reaction Time and Speed of Movement Tests We tested reaction times and speed of movement using the sensorimotor interface hand module. c All participants were tested according to the protocol provided by the manufacturer. 30 The tests consisted of simple reaction time (SRT), 1-target reaction time (RT1) and speed (SOM1), and 2-target reaction time (RT2) and speed (SOM2). Reaction times were measured in milliseconds as the time delay between a light stimulus and the release of the hand from the center plate (fig 2). In the simple reaction task, participants were asked to move their hand off the plate in reaction to a light stimulus. The other reaction time tests required hand movements from the center plate toward the plate with the light stimulus, given either 1 (RT1) or 2 (RT2) possible targets. Movement speed (in cm/s) was calculated by dividing the distance between the center and target plates by the time taken for hand movement from 1 plate to the other. Characteristic Lateral Epicondylalgia Controls Men/women (n) 24/16 24/16 Age (range), y 49.5 (32 66) 48.4 (33 64) Duration of lateral epicondylalgia (mo) NA Side Affected Dominant* Dominant Right Left Grip Affected Unaffected Nondominant Dominant MGS (N) PFGS (N) NA NA NA NOTE. Values are mean standard deviation. Abbreviations: MGS, maximum grip strength; NA, not applicable; PFGS, pain-free grip strength. *Sixty percent of affected elbows were on the dominant side (right 22, left 2). Fig 2. Sensorimotor measures of upper-limb reaction time and speed of movement were tested using the sensorimotor interface hand module of the Basic Elements of Performance c system.

3 492 SENSORIMOTOR ABNORMALITIES IN EPICONDYLALGIA, Bisset Pain Intensity Each participant in the lateral epicondylalgia group was asked to indicate the level of pain experienced on a visual analog scale (VAS) during the maximal gripping task on the affected side. This VAS was anchored with no pain (0mm) and worst pain imaginable (100mm) and the distance in millimeters along the line was manually recorded. Procedure We tested using a predetermined sequence: tests for reaction time and speed of movement were performed first (SRT, RT1 SOM1, RT2 SOM2), followed by the measures of wrist posture and grip strength. Maximal grip strength and VAS of the affected side were measured last in the lateral epicondylalgia group. The order in which each side was tested in the control group was randomized using a computer. In the lateral epicondylalgia group, the unaffected side was always measured first to facilitate familiarization with the measurement. 28 Reliability of Measures Upper-limb reaction time, speed of movement, and grip strength measures have been shown to be reliable and are useful measures in the study of lateral epicondylalgia. 17,28,31-33 The validity and reliability for the measure of joint angle from a digital image b has been previously established for the knee. 29 The methods used for the knee were modified to measure wrist angle in the sagittal plane during a grip strength test. The method to measure wrist posture was developed specifically for this study and as such, its test-retest reliability and measurement accuracy were evaluated prior to the main study. To evaluate the accuracy of the new measure of wrist angle, it was compared with a standard 30cm universal goniometer. 34 A series of angles were measured from the goniometer, which ranged from 10 to 10 in steps of 5, with parallax error induced by rotation evaluated by rotating the goniometer about its longitudinal axis from 10 to 10 in 5 increments for each goniometric angle measured. The digital camera was aligned visually with the axis of the goniometer and a digital image recorded for each angle. The goniometer angle was recorded manually at the time the digital photograph was taken by an assistant. The image was then downloaded onto a computer and the angle measured. The rater of the digital image was blind to the goniometer angle. The clinically acceptable variation between the new method and the goniometer was set at 1, because this is the smallest increment of measure on the universal goniometer device. Using the Bland and Altman 35 method of agreement, the absolute mean difference between the 2 devices was.35 with limits of agreement from.20 to.89, which were within the previously specified (1 ) clinical criteria of accuracy. When compared with the standard method of measurement in clinic (ie, the universal goniometer) the new digital measure of joint angle was considered acceptable. That is, the position of the arm-forearm segment could vary by 10 rotation about its longitudinal axis without producing an unacceptable error in the measurement of sagittal plane angulation of the wrist joint. It is reasonable to assume forearm position error would be well within 10 during measurement, considering that upper-limb joint position error has previously been reported to be approximately 2. 36,37 To evaluate intertester reproducibility of the wrist posture measures, 2 assessors who were blind to each other s measures assessed the wrist angle on 9 participants. Intraclass correlation coefficients (ICCs) and standard error of the measure (SEM) were calculated to assess reliability. The ICC 2,2 was.786 with an SEM 1.86, thus demonstrating satisfactorily high agreement between testers. 38 Two raters in the main study were blind to each other and each measured wrist angles for only 1 group (ie, either lateral epicondylalgia or control) to control for bias. Data Analysis Data were expressed as mean and 95% confidence intervals (CIs), and were plotted to highlight comparisons. Mixed multivariate analysis of variance (MANCOVA) evaluated effects of group (lateral epicondylalgia, control), sex (men, women), and side (affected, unaffected or dominant, nondominant) with the covariate of age on dependent variables of wrist angle, grip strength, reaction times, and speed of movement. Alpha was set at.05. Significant interaction effects from the omnibus analyses were further evaluated by tests of simple effects and displayed as mean differences and their 95% CI. Pearson coefficients were used to evaluate relationships between pain indices and other variables in the lateral epicondylalgia group. RESULTS The results of the MANCOVA revealed that there was no effect of age, sex, or dominance (side) on all dependent variables, except for the effect of sex on maximum grip strength for both lateral epicondylalgia and control groups and the effect of sex on SOM2 for the control group. Data for the dependent variables of wrist angle, maximum grip strength, reaction time, and speed of movement were collapsed in comparisons between lateral epicondylalgia and control groups, because there was no effect for side. Results are presented according to the dependent variables. Wrist Angle The amount of wrist extension adopted by the lateral epicondylalgia group during grip testing was less than the control group (P.001). The mean difference in wrist angle between the lateral epicondylalgia group and the control group was significant (11 ; 95% CI, 7 14 ). There was no effect of age, sex, or side on adopted wrist angle (P.05), the latter indicating the deficit was bilateral. Grip Strength In the lateral epicondylalgia group, pain-free grip strength (affected side) was significantly less than maximal grip strength on both the same (mean difference, 98N; 95% CI, N) and unaffected sides (mean difference, 170N; 95% CI, N). Comparison between groups revealed that maximum grip strength on the unaffected side of the lateral epicondylalgia group was significantly greater than in the control group (mean difference, 44N; 95% CI, 8 80N). There was no significant difference in maximum grip strength between the control group and the affected arm of the lateral epicondylalgia group (mean difference, 28N; 95% CI, 8.5 to 65N; P.13). A significant effect of sex (favoring men) on maximum grip strength was apparent in the control group (mean difference, 96N; 95% CI, N), as well as on maximum grip strength in the lateral epicondylalgia group on both the unaffected (mean difference, 109N; 95% CI, N) and affected sides (mean difference, 64N; 95% CI, N). Figure 3 highlights this effect. Sex did not influence pain-free grip strength (mean difference, 24N; 95% CI, 13 to 60N).

4 SENSORIMOTOR ABNORMALITIES IN EPICONDYLALGIA, Bisset 493 Table 2: Mean Difference Between Groups for SRT, RT1, and RT2 and SOM1 and SOM2 Dependent Variable Mean Difference Lower 95% CI Upper % Absolute Difference SRT (ms) RT1 (ms) RT2 (ms) SOM1 (cm/s) SOM2 men (cm/s) SOM2 women* (cm/s) NOTE. All data are averaged between sides, because there was no effect for side (P range, ) in either group for any of the measures, with the exception of SOM2. SOM2 exhibited an effect for sex in the control group (P.02) and is therefore presented by sex. A positive difference in reaction time and a negative difference in speed of movement indicate a shorter reaction time and faster speed in favor of the control group, respectively. Differences are all expressed as percentage absolute differences. *Not significant (P.05). Fig 3. Mean grip force and 95% CIs for lateral epicondylalgia (, men;, women) and control (grey horizontal bands) groups by sex. The mean for women controls was 182 (95% CI, ) and men controls 278 (95% CI, ), respectively. Black data points represent the affected side and the white data points represent the unaffected side. Reaction Time and Speed of Movement The predominant finding for the reaction time and speed of movement data was a significant main effect for group; that is, lateral epicondylalgia versus control (fig 4, table 2). Reaction times in the lateral epicondylalgia group were delayed by 11% to 13% (P.001) and speed of upper-limb movement was reduced on average 2% to 15% (P range, ). There was no effect of age, side (ie, dominance vs nondominance, affected vs unaffected), or sex in either group except for Fig 4. Measures of motor performance derived from the Basic Elements of Performance device. Triangle data points are mean (with 95% CI) reaction time measures (primary axis) and square data points are mean (with 95% CI) speed of movement (secondary axis) measures. Black data points are lateral epicondylalgia group and white hatched points are the control group. All data are averaged between sides as there was no significant effect of side, except for SOM2 in the control group, which differed significantly between sexes in the control group: the large white square data point is the control men and the small white square data point is the control women. controls, in which there were differences in the way sex differentiated SOM2. SOM2 for the lateral epicondylalgia group was significantly slower than the control men by 15.5% but only 2% slower than the control women, which was not statistically significant (see table 2). Pain Intensity The mean level of pain (VAS) perceived during the maximum grip strength on the affected side was 55.63mm (95% CI, mm). There was a weak to moderate correlation between the pain intensity and force exerted during pain-free grip strength tests (Pearson r.442, P.004). Pain intensity did not correlate significantly with any other variable. DISCUSSION This study is the first to evaluate wrist posture, upper-limb reaction time, speed of movement, and grip strength concurrently in lateral epicondylalgia across all measured indicators of motor performance. The lateral epicondylalgia group performed the grip test in a relatively flexed wrist posture and had slower reaction times and speed of movement of the upper limb when responding to a visual stimulus. These findings were bilateral: that is, not only were there deficits on the affected side, but on the majority of measures, the unaffected side was also significantly impaired. Participants with lateral epicondylalgia adopted a relatively flexed wrist posture when performing a simple grip task, which to our knowledge has not been previously reported. The simple grip task that was evaluated in this study plays an important role in normal daily activities. Gripping in a flexed wrist posture has been shown to be inefficient in producing maximum grip force in normal populations This inefficiency was exhibited by force deficits in the order of 40% to 50% occurring concurrently with increased electromyographic activity of forearm flexors and extensors. 24 Analysis of the grip strength revealed 2 striking features in the lateral epicondylalgia group. Foremost is that the maximum grip strength on the unaffected side of the lateral epicondylalgia group was significantly greater than that of the control group. There are several explanations we propose for this unexpected finding. One reason may be that the greater grip strength in the lateral epicondylalgia group could have developed on the unaffected side, as a compensatory strategy to protect the injured arm. This may be a result of muscle system

5 494 SENSORIMOTOR ABNORMALITIES IN EPICONDYLALGIA, Bisset adaptation to greater demands imposed on the uninjured arm from a reduction of usage of the injured arm. Another plausible explanation is that the lateral epicondylalgia group was stronger on grip strength than the control group prior to developing lateral epicondylalgia. The exact significance of this finding requires further investigation. It is well known that patients with unilateral lateral epicondylalgia exhibit unilateral pain-free grip strength deficits, 18-20,39 another finding of grip strength substantiated by this study. The mean deficit in pain-free grip strength in this study was 170N, or 60% of the unaffected side, which is comparable to those seen in other studies (Sran et al, 39 54% deficit; Stratford et al, 20 48% 58% deficit). There was a sex difference in maximum grip strength for both the control group and the unaffected side of the lateral epicondylalgia group, with men being stronger (see fig 3). This was not evident in the affected lateral epicondylalgia pain-free grip strength. Interestingly, the absolute deficit in pain-free grip strength was greater within men than within women. Closely mirroring the wrist angle deficits were the slower reaction times and speed of movement. Pienimaki et al 21 studied reaction times and speed of movement in 32 lateral epicondylalgia patients with age- and sex-matched controls and reported deficits of 19% to 36% for reaction time and 31% for speed of movement. Some possible reasons for the differences in magnitude of findings between the 2 studies are that the lateral epicondylalgia group of Pienimaki 21 was younger (mean, 43y vs 49y in our study), predominantly women (21/32 [66%] vs 16/40 [40%] in our study) and had had the condition for a median of 31 months (our study median duration of condition, 4.5mo). Because there was no sex or age effect in our sample, it would appear that the chronicity of the condition may be responsible for the effect size differences between studies. It is inviting to speculate about the underlying mechanism of the observed bilateral changes in the motor tasks tested herein. Evidence is emerging of interhemispheric transfer of information between homologous cortical areas during a unilateral motor task in the normal population regardless of hemisphere dominance. 40,41 Perhaps through a mechanism of interhemispheric communication the impaired motor task on the injured side is mapped onto the uninjured side. Alternatively, altered motor control may have been a precursor to lateral epicondylalgia. Further work is required to evaluate this. CONCLUSIONS A new finding in lateral epicondylalgia of bilateral differences in adopted wrist posture during gripping has been identified. 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