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CLINICAL SCIENCES

An Investigation of the Asymptomatic Limb in Unilateral Lateral Epicondylalgia

HEALES, LUKE J.; HODGES, PAUL W.; VICENZINO, BILL

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Medicine & Science in Sports & Exercise: November 2015 - Volume 47 - Issue 11 - p 2268-2272
doi: 10.1249/MSS.0000000000000681
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Abstract

Lateral epicondylalgia (LE) affects the common extensor tendon of the elbow (22) and is associated with local tendon abnormalities identified with musculoskeletal ultrasound (MSUS) imaging (19). The purported relation between pain and imaging findings is complicated by the observation that tendinopathy-like changes are present on the contralateral asymptomatic side in people with some unilateral tendinopathies (13). For example, an animal model of repetitive unilateral exercise demonstrated Achilles tendon pathology in the form of increased tenocyte count and neovascularity in both the exercised (injured) and the nonexercised limbs (1). This was consistent with human data, in which the asymptomatic limb of a group with unilateral Achilles tendinopathy (AT) demonstrated greater tendon thickness and less echogenicity on MSUS imaging than disease-free controls (11). On the basis of sensory and motor deficits on the asymptomatic side that have been revealed in a recent systematic review (13), we predicted that there would be MSUS changes in the asymptomatic elbow of people with unilateral LE. The aim of this study was to use MSUS imaging to assess the common extensor tendon for signs of tendon pathology, including grayscale features and neovascularization, in the symptomatic and contralateral asymptomatic limb of participants with clinically diagnosed unilateral LE and to compare the incidence of tendon changes between people with LE and age-, sex-, and arm dominance-matched controls with no history of LE.

METHODS

Participants

Twenty-nine participants with unilateral LE and 32 pain-free controls, matched for age, sex, and arm dominance, were recruited as part of a previously published article investigating the diagnostic accuracy of MSUS in people with unilateral LE (12). Inclusion criteria for unilateral LE were presence of pain over one lateral epicondyle for greater than 6 wk that was provoked by palpation, resisted wrist and middle finger extension, and gripping. Participants were excluded if they had any major neurological or systemic conditions (e.g., epilepsy, diabetes), limited range of movement (neck or arm), bilateral elbow symptoms, or previous treatment. Pain-free controls were included if they had no history of elbow pain and no major or systemic disease. Participants were excluded from either group if they had neck or arm pain (other than LE, for the LE group), which had prevented participation in work or recreational activities, or required consultation by a health care practitioner in the past 6 months. Participants with LE were all right side-dominant, and in all participants, the dominant side was symptomatic. The Institutional Medical Research Ethics Committee approved the study, and a written informed consent was obtained before participation.

Characterization of the LE group

Clinical measures including the patient-rated tennis elbow evaluation (PRTEE), grip strength dynamometry, and numerical rating scale (NRS) for pain intensity were recorded to characterize the LE group (Table 1). The validated PRTEE is specific to LE and involves 15 questions that measure pain severity and functional disability, with the total providing an overall score from 0 to 100 (higher score implies greater pain and disability) (24). The 11-point NRS (0, no pain; 10, worst pain imaginable) was used to assess worst pain intensity over the preceding week. An electronic grip dynamometer (MIE Medical Research Ltd., Leeds, United Kingdom) was used to measure pain-free grip force. Participants were instructed to cease gripping at the first onset of pain (20). Healthy controls were required to grip the dynamometer with maximal force, as they experienced no pain. Grip force was measured in the supine position, with the elbow extended beside the body and the forearm pronated with the palm facing down (6,20).

TABLE 1
TABLE 1:
Participant characteristics and demographics.

MSUS imaging procedure and interpretation

MSUS examinations were performed bilaterally by one of two qualified musculoskeletal sonographers, each with over 9 yr experience. This examination only considered the common extensor tendon (the radial collateral ligament was identified and excluded from the examination), but we acknowledge that the radial collateral ligament may also be degenerative in both patient and controls (14). Sonographers were blind to the clinical examination results and group allocation (LE or control). To establish intertester reliability, both sonographers scored nine participants independently. Intertester reliability of grayscale features and neovascularity has been previously reported (12). Intertester reliability of tendon thickness (mm) and hypoechoic volume (mm3) is reported in the Results section. Sonographers used a standardized protocol including imaging the tendon in the longitudinal and transverse planes to assess for grayscale features indicative of tendinopathy followed by neovascularization in the right then left arm. Participants sat with the arm supported in 70° of elbow flexion and the wrist in neutral position.

Grayscale imaging was performed using a linear array transducer with a frequency range of 5–17 MHz (Philips IU22 Ultrasound; Philips Medical Systems, Bothell, WA) to assess tendon thickening, hypoechoic region/s, fibrillar disruption, and calcification using a previously established scoring system (23). Individual grayscale features were assigned an ordinal grade using a four-point scale of increasing abnormality (0, normal; 1, only just apparent; 2, visible in less than half the tendon; and 3, visible in more than half the tendon) (23). The sum of the individual grayscale features was used to calculate a total “grayscale score” with a maximum rating of 12. Power Doppler imaging was used to identify intratendon neovascularity using a pulse repetition frequency of 500 Hz, wall filter of 40 Hz, and preset color gain of 80%. Neovascularity was scored using a five-point ordinal scale (0, normal; 1, single small signal; 2, several signals visible in less than 33% of the tendon; 3, multiple signals visible in 33%–66% of the tendon; and 4, multiple signals in more than 67% of the tendon) (23). The scoring of grayscale features and neovascularity using the ordinal scales was based on the subjective judgment of the sonographers. Objectively, we also measured tendon thickness in millimeters using built-in software by placing a marker on the borders of the tendon in the longitudinal plane. Hypoechoic volume was measured in cubic millimeters using built-in software by placing markers around the lesion of interest in both the longitudinal and transverse planes.

Statistical analysis

Statistical analysis used Statistica Software (StatSoft, Inc., Tulsa, OK). A two-way repeated-measures ANOVA was used to compare measures between groups (LE vs pain-free control) and sides (dominant vs nondominant). Post hoc analysis used the Duncan multiple range test. Student’s t-tests were used to assess for differences of participants’ characteristics between groups. Significance was set at 0.05. Group data are described as mean and SD as well as mean differences and their 95% confidence intervals (CI), where appropriate. A two-way mixed intraclass correlation coefficient (ICC) with absolute agreement was used to determine the intertester reliability for the measures of tendon thickness and the volume of the hypoechoic region. Kappa statistics was used to assess the intertester reliability for grayscale and neovascular changes. On the basis of established criteria, the intertester reliability was interpreted as slight (0.0–0.2), fair (>0.2–0.4), moderate (>0.4–0.6), substantial (>0.6–0.8), or almost perfect (>0.8–1.0) (18).

RESULTS

Intertester reliability

Intertester reliability revealed moderate to almost perfect agreement between the two musculoskeletal sonographers for grayscale changes, tendon thickening (κ = 0.68), hypoechoic region (κ = 0.80), fibrillar disruption (κ = 0.58), and calcification (κ = 0.44). Neovascularity was almost perfect (κ = 0.86), and both tendon thickness (ICC, 0.95 (95% CI, 0.87–0.98)) and hypoechoic volume (ICC, 0.82 (95% CI, 0.56–0.93)) were almost perfect.

MSUS examination

The score for tendon thickening, hypoechoic change, fibrillar disruption, calcification, and neovascularity did not differ between the contralateral asymptomatic elbow of the LE group and the matched arm (nondominant) of the pain-free controls (Table 2). The symptomatic elbow (dominant) of the LE group revealed a higher score for tendon thickening, hypoechoic change, fibrillar disruption, and neovascularization but not for calcification, when compared with that in the matched elbow (dominant) of the pain-free controls and the contralateral asymptomatic elbow of the LE group (Table 2).

TABLE 2
TABLE 2:
The mean (SD) and mean difference and 95% CI between groups for scores of tendon thickening, hypoechoic changes, fibrillar disruption, calcification, and neovascularization.

The measures of tendon thickness and hypoechoic volume did not differ between the contralateral asymptomatic elbow (nondominant) of the LE group and the matched elbow (nondominant) of the pain-free controls (Table 3). In addition, the symptomatic elbow (dominant) of the LE group was not thicker than the matched elbow (dominant) of the pain-free controls; however, the symptomatic (dominant) elbow of the LE group was thicker than the contralateral asymptomatic (nondominant) elbow of the LE group (Table 3). The symptomatic elbow (dominant) of the LE group revealed a greater hypoechoic volume than the matched elbow (dominant) of the pain-free controls and the contralateral asymptomatic elbow (nondominant) of the LE group (Table 3).

TABLE 3
TABLE 3:
The mean (SD) and mean difference and 95% CI between groups for tendon thickness (mm) and hypoechoic volume (mm3).

DISCUSSION

Using MSUS imaging, this study identified features of tendinosis in the symptomatic elbow of people with clinically diagnosed unilateral LE. Although many participants with LE revealed tendon changes on the contralateral asymptomatic side, the incidence of tendon abnormality was not greater than that of pain-free controls with no history of elbow pain, which is contrary to observations from other tendinopathies (11). This finding does not support the hypothesis of significant tendon changes in the asymptomatic common extensor tendon, which was predicted on the basis of evidence of bilateral tendon changes in rabbits that performed exercise of a single limb (1), bilateral tendon changes in humans with unilateral AT (11), and the bilateral nature of numerous other sensory and motor system changes in LE (13).

Some features of tendinopathy were not greater in the symptomatic elbow in LE

Calcification is often considered a feature of tendinopathy (16). We did not observe significant between-group differences in the symptomatic elbow for calcification (calcification was observed in only five of 29 (17%) symptomatic elbows in people with unilateral LE and only six of 32 (18%) matched elbows of the pain-free controls). The absence of calcification in the symptomatic arm concurs with the results of a recent systematic review that reported that calcification is not consistently found in the common extensor tendon of people with LE (8).

In addition, our study did not identify differences between the symptomatic (dominant) elbow of the LE group and the matched arm of the pain-free controls (dominant) (Table 3) and the mean difference was within the SE of the measure (0.29 mm). This differs from previous work that has reported greater tendon thickness in the symptomatic elbow of people with LE compared with that in a control group (2,19), but that previous work did not blind the sonographers to the participant group (2,19). MSUS imaging has the potential for bias because of the potential subjectivity of the scoring (2,19). This might lead to error in the collection and interpretation of images. Sonographers in the present study were blinded to the group allocation (LE vs controls) and revealed almost perfect intertester reliability for tendon thickness. This strengthens our observations.

We identified a significant difference in tendon thickness measure (mm) between the symptomatic and asymptomatic elbow of the LE group, which was greater than the SE of the measure. The explanation of this difference in the absence of no difference between the symptomatic arm of people with LE and the matched arm of the pain-free controls is not clear. It might suggest that people with LE do not have bilateral changes and increased thickness might indeed be a feature at the symptomatic tendon that is not observed between patients and controls.

Tendon pathology in healthy controls

The presence of tendon changes (observable with MSUS imaging) in 49% (31 of 64 elbows showed a total grayscale and neovascularization score of ≥2) of the pain-free control participants, despite the absence of symptoms, requires consideration. These changes may represent subclinical pathological change, a reflection of normal variation in tendon quality (and not reflective of frank pathology), or error in the measurement based on the clinical judgment required by the sonographer. There is precedence to expect that subclinical pathological change might be a precursor to symptomatic tendinopathy (5,9). Longitudinal studies have revealed that elite athletes with an abnormal Achilles or patellar tendon, as measured by MSUS imaging, had a greater chance of developing symptomatic tendinopathy than those without tendon changes (with tendon changes, 45% and 22%, vs without tendon changes, 1% and 7%, for Achilles and patellar tendons, respectively) (5,9). Tendon pathology of the common extensor origin in 12%–13% of asymptomatic individuals has been validated with MSUS imaging, and this is greater in the dominant arm and with increasing age (15,27). Jaén-Díaz et al. (15) revealed that 85% of people with asymptomatic tendon pathology were older than 40 yr. In the current study, 29 (91%) of the 32 pain-free controls were 40 yr or older, which might explain the high proportion of tendon abnormality.

The accuracy of methods to identify tendon changes might contribute to the differences between studies. Human biopsies have been used to study pathology in the patellar tendon of asymptomatic individuals undergoing surgical repair of anterior cruciate ligament injury (4). Although this technique is likely to be the most accurate method to confirm/refute the presence of pathology, no studies have harvested biopsies of the asymptomatic limb; thus, no comparison to an asymptomatic side is available. Most studies have used MSUS to identify tendon pathology; however, because sonographic imaging depends on sonographer interpretation (2,7,19), care must be taken to control for bias. We took several steps to limit bias and control for the variability in the collection and interpretation of the images, and all measures had moderate to almost perfect intertester reliability. Critically, the sonographer was blinded to the injury status of the participant and used a standardized protocol for image interpretation (25). Previous investigation of AT in humans that found deficits in the asymptomatic and symptomatic limb compared with a control did not blind the sonographer (11). This highlights the possibility that a lack of blinding might have influenced the interpretation of the MSUS images. In addition, factors such as genetics (21), exercise (28), diabetes (10), and adiposity (10,26) have been suggested to lead to dysmorphic tendon structure. Because neither study controlled for these factors, it is not possible to speculate about whether they explain different outcomes.

There are several possible explanations for the contrasting observations that bilateral tendon changes are not see in LE but are seen in other tendinopathies. First, LE may have a different mechanism from other tendinopathies (e.g., Achilles tendon (11)). Sonographically detected tendon abnormality depends on load (17,28). By nature of human function, each of the lower limbs are more likely to be exposed to similar loads/stress (e.g., gait) than the upper limbs, which may each be exposed to asymmetrical load/stress (e.g., dominant arm used for holding a tennis racket). Second, tendon abnormalities in the asymptomatic limb might be related to the duration of symptoms. The duration of symptoms for participants in the present investigation was approximately half that of previous work in AT (11). Third, only male participants were recruited in the study of AT (11). Although our study found no sex differences, there may have been subtle individual changes in females, secondary to mechanisms such as protective effects of estrogen on tendons (3). Further investigations are required to better understand differences between tendons in LE and others.

CONCLUSIONS

This study did not demonstrate greater prevalence of sonographic abnormalities in the asymptomatic elbow of people with unilateral LE than the elbows of asymptomatic controls. This does not support predictions formed from previous research demonstrating tendon pathology in the asymptomatic tendon of people with AT compared with controls and in biopsies of the nonexercised tendon in an animal model. Further research on LE and other tendinopathies, controlling for issues such as assessor blinding and associated risk factors, is required to better understand the development of asymptomatic tendon pathology in unilateral tendinopathy.

The authors would like to acknowledge Mr. S. Blackwell, Dr. A. Chan, Ms. A. Lacey, and Ms. K. Place from CitiScan Radiology.

Funding was provided by a program grant from the National Health and Medical Research Council of Australia (ID631717). P. H. is supported by a Senior Principal Research Fellowship (APP1002190), and L. H., by an Australian Postgraduate Award scholarship.

The authors declare no competing interests. The results of the present study do not constitute endorsement by the American College of Sports Medicine

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Keywords:

TENNIS ELBOW; BILATERAL; MOTOR SYSTEM; ULTRASOUND; IMAGING

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