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Bilateral Cervical Dysfunction in Patients With Unilateral Lateral Epicondylalgia Without Concomitant Cervical or Upper Limb Symptoms: A Cross-Sectional Case-Control Study
BILATERAL CERVICAL DYSFUNCTION IN PATIENTS WITH UNILATERAL LATERAL EPICONDYLALGIA WITHOUT CONCOMITANT CERVICAL OR UPPER LIMB SYMPTOMS: A CROSS-SECTIONAL CASE-CONTROL STUDY Brooke K. Coombes, PhD, a Leanne Bisset, PhD, b and Bill Vicenzino, PhD a
ABSTRACT Objective: The purposes of this study were to examine the prevalence and distribution of spinal and neurodynamic dysfunction in a population with unilateral lateral epicondylalgia (LE) without concomitant cervical or upper limb symptoms, compare with cervical examination in a healthy control population, and investigate potential associations with clinical and demographic factors. Methods: This cross-sectional study included 165 patients with LE along with 62 healthy controls. Manual examination (C4-T2) was performed by an unblinded examiner with dysfunction defined as pain of 3 or higher on a numerical rating scale in the presence of a severe or moderate hypomobility or hypermobility. Neurodynamic testing (radial nerve) was classified positive if LE symptoms were reproduced and altered by sensitization maneuver. Repeated-measures analysis of variance was used to compare sides, segmental levels, and groups. Regression analysis was used to determine associations between variables. Results: Thirty-six percent of patients had dysfunction of at least 1 spinal palpation site, and 41% had a positive neurodynamic test. Significant group-by-level (P = .02) and group-by-side (P = .04) interactions were found for spinal examination, with greater dysfunction bilaterally at C4-7 (P b .01) in LE compared with control arms. The number of positive palpation sites was associated with injury duration (P = .03), whereas neurodynamic response was associated with severity of resting pain (P = .04). Conclusions: Cervical dysfunction is evident in individuals with LE without obvious neck pain and may reflect central sensitization mechanisms. Further study of the nature of the relationship between cervical dysfunction and LE is required. (J Manipulative Physiol Ther 2014;37:79-86) Key Indexing Terms: Tennis Elbow; Neck Pain; Radial Nerve; Musculoskeletal Manipulations
ateral epicondylalgia (LE), also known as tennis elbow, is empirically considered a tendinopathy of the extensor carpi radialis brevis origin. 1 However, there is also recognition of a relationship between the cervical spine, radial nerve, and LE. 2,3 First, there are findings of a greater prevalence of neck pain in patients with lateral elbow pain compared with an age-matched control population 4 as well as greater radial nerve
L a
Researcher, School of Health and Rehabilitation Sciences, University of Queensland, St Lucia, Queensland, Australia. b Researcher, Griffith Health Institute, Griffith University, Gold Coast, Queensland, Australia. Submit requests for reprints to: Bill Vicenzino, PhD, Therapies Building 84A, University of Queensland, St Lucia 4072, Queensland, Australia (e-mail: [email protected]). Paper submitted July 16, 2013; in revised form September 12, 2013; accepted September 20, 2013. 0161-4754/$36.00 Copyright © 2014 by National University of Health Sciences. http://dx.doi.org/10.1016/j.jmpt.2013.12.005
mechanosensitivity of the affected arm in patients with unilateral symptoms. 3,5 Others have found widespread pain over the neck or upper limb to commonly coexist alongside chronic epicondylitis, with widespread symptoms being associated with chronicity. 6 Secondly, poorer long-term prognosis is predicted by self-reported neck pain, independent of high baseline lateral elbow pain intensity. 7 Juxtaposed upon this is evidence of the effectiveness of manual therapy directed toward the cervicothoracic spine in conjunction with elbow treatment, including benefit in previously recalcitrant cases, 8 fewer treatment sessions, 9 and greater improvement in short-term pain. 10 However, only the latter pilot study of 10 participants was a randomized trial, highlighting that more research in this area is needed. With estimates ranging from 57% to 90%, 4,11,12 the true prevalence of related cervical spine and radial nerve pathology in the LE population has not been conclusively established. Differences in eligibility criteria, examination procedure, and criteria used to detect dysfunction provide 79
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Fig 1. Flow chart for selection of LE and control participants. Data for the LE group were collected before enrollment into a randomized controlled trial, 13 the methodology for which is described in detail elsewhere. 14
strong sources of heterogeneity between studies. Moreover, the presence of cervical dysfunction may be seen as a differential diagnosis from true LE 2 or as a subgroup thereof. The extent and distribution of spinal and neurodynamic dysfunction in LE individuals without concomitant neck or other upper limb symptoms have not been previously evaluated and provide a logical step for this field of interest. This study aimed to evaluate whether there are differences in manual examination of the cervical and thoracic spine between LE patients and healthy controls who did not have additional (or concomitant) neck or upper limb symptoms. Second, the relationships between spinal manual examination, radial nerve neurodynamic test responses and pain severity, duration of injury, age, and sex were studied to further shed light on potential mechanisms.
METHODS Design This cross-sectional, comparative study investigated the prevalence of abnormal findings from a clinical examination of the cervical and thoracic spine and radial nerve in individuals with and without unilateral LE (Fig 1). Data for the LE group were collected before enrollment into a randomized controlled trial, 13 the methodology for which is described in detail elsewhere. 14
Participants All patients were recruited from the greater Brisbane region of Australia through community media advertisements. Eligibility was determined by a 2-stage process (telephone interview and physical examination) by 1 researcher (BKC) and confirmed by a second researcher (BV). 14 One hundred sixty-five patients with a clinical diagnosis of LE, meeting the following criteria, were included: unilateral elbow pain over the lateral epicondyle for longer than 6 weeks and pain provoked by at least 2 of the following: gripping, palpation, resisted wrist or middle finger extension, or stretching of forearm extensor muscles with reduced pain-free grip. Exclusion criteria were recent injection or physiotherapy, neck or other upper limb symptoms necessitating treatment or preventing participation in usual work or recreational activities in the preceding 6 months, exacerbation of elbow pain with neck examination (ie, active and passive motion, palpation), sensory disturbance of the hands, fractures, elbow surgery, malignancy or inflammatory disorders, pregnancy, breastfeeding, or contraindication to injection. Sixty-two healthy control participants aged 35 to 70 years were included. Exclusion criteria for control participants were history of LE and neck or other upper limb symptoms necessitating treatment or preventing participation in usual work or recreational activities in the preceding 6 months. Ethical approval was granted by the
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institutional review board (University of Queensland), and informed written consent was obtained from all patients. This trial was supported by the Australian National Health and Medical Research Council grant 511238. Coombes was in receipt of a University of Queensland Research Scholarship.
Outcome measures The tests used in this study were selected because of their frequent use in clinical assessment of the neck and upper limb. All testing was completed by a single physiotherapist (BKC) with a postgraduate degree in musculoskeletal physiotherapy who was not blinded to whether the subject had LE. Spinal manual examination was performed on all patients, whereas neurodynamic function was evaluated in LE patients only. Patients were asked to rate the level of elbow pain currently experienced at rest and the worst level of pain experienced during the past week on 100-mm visual analog scales (VAS) with the following end points: no pain (0 mm) and worst pain imaginable pain (100 mm). Manual Examination. Intersegmental manual examination or passive motion palpation of the cervical and thoracic spine was performed between C4 and T2 segments bilaterally on all patients in prone lying. The examiner rated the intersegmental end feel on a previously defined scale, 15 ranging from 1 (severe hypomobility) to 7 (severe hypermobility), with 4 representing normal mobility. Previous study of the reliability of this method in participants with cervicogenic headache or migraine and a control group reported high κ values. 15 The participant also verbally rated any pain provoked by examination on an 11point numerical rating scale. A positive response was recorded at each of the 10 sites (5 levels × 2 sides) based on the following criteria: moderate to severe hypomobility or hypermobility (ie, scores of 1.2 and 6.7, respectively) along with a pain response of 3 or greater. 15 An aggregate score (range, 0-10), consisting of the sum of positive palpation sites, was also derived for further analyses. We based the criteria for dysfunction on assessment of both the quality of passive segmental motion as well as provocation of pain, due to the qualitative nature of assessment of joint motion alone. 16-18 Previous review of the reliability of static spinal palpation found that acceptable κ values were more common for studies evaluating pain provocation, although no one method could be deemed clearly superior. 19 Neurodynamic Examination. The upper limb neurodynamic test (ULNT) for the radial nerve was performed as previously described, 20 using the following sequencing: shoulder girdle depression, elbow extension, shoulder internal rotation, pronation, wrist and finger flexion, and shoulder abduction to the end of range or until symptoms were produced (Fig 2). Once such a sensation was provoked, structural differentiation between neurogenic and nonneurogenic sources of pain was performed by the addition of sensitizing move-
Fig 2. Upper limb neurodynamic test with radial nerve bias, comprising shoulder girdle depression, elbow extension, shoulder internal rotation, pronation, wrist and finger flexion, and shoulder abduction, followed by sensitizing movements of shoulder girdle elevation or cervical lateral flexion. (Color version of figure is available online.)
ments at a site distant to the pain (shoulder girdle elevation or cervical lateral flexion) while all other test components were maintained. Based on a previous study evaluating the validity of the ULNT, 21 the test was considered positive if the following 2 criteria were present: (1) the subject's symptoms were reproduced at least partially, and (2) symptoms were altered by structural differentiation. Moderate reliability (κ = 0.44) has been reported for the radial nerve ULNT using the above criteria. 22
Data Analysis This study was powered to detect differences between LE and control participants based on measures not evaluated in this study, including quantitative sensory testing, anxiety, and depression, the results of which are published elsewhere. 23,24 Statistical analysis was performed using SPSS 20 (IBM, Somers, NY), with a P b .05 significance level. Manual examination of the cervical and thoracic spine was compared between LE and control groups using repeated-measures analysis of variance, including the within-subject factors of side (ipsilateral or contralateral) and level (C4-5, C5-6, C6-7, C7-T1, or T1-2) and the covariates age and sex. Control patients were randomly allocated a “matched” affected arm, referred to herein as the ipsilateral arm, such that the control group had an equivalent proportion of dominant-sided arms as that observed in the LE group to account for any potential influence of hand dominance. Linear regression was used to evaluate potential associations of severity of pain, age, sex, and duration on the aggregate score of manual examination, that is, the sum
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Table 1. Baseline characteristics of LE and control participants LE (n = 164) Controls (n = 62) Age (y) Female Body mass index Manual occupation Sport involving strong gripping Duration of symptoms (wk) Incident cases Dominant arm affected Worst pain (VAS: 0-100) Current resting pain (VAS: 0-100) Pain and disability (PRTEE: 0-100) Pain-free grip (N)
49.6 ± 9.0 63 (38.4%) 26.5 ± 5.1 41 (24.8%) 58 (35.2%) 25.1 ± 29.8 125 (76.2%) 116 (70.7%) 61.9 ± 18.4 10.8 ± 13.4 39.5 ± 14.1 150.7 ± 128.4
49.6 ± 8.7 28 (45.2%) 25.4 ± 4.7 12 (19.4%) 14 (22.6%)
Data represent mean ± SD or count (percentage). LE, lateral epicondylalgia; VAS, visual analog scale.
of positive spinal palpation sites. Logistic regression was used to evaluate the relationship of these factors on the ULNT response. All variables were simultaneously entered into each model.
Table 2. Results of spinal manual examination in LE and control patients Segmental level
Side
LE (n = 164)
Controls (n = 62)
C4-5
Ipsilateral Contralateral Ipsilateral Contralateral Ipsilateral Contralateral Ipsilateral Contralateral Ipsilateral Contralateral
19 (11.6%) 17 (10.4%) 31 (18.9%) 18 (11.0%) 29 (17.7%) 8 (4.9%) 8 (4.9%) 4 (2.4%) 4 (2.4%) 2 (1.2%)
1 2 2 2 1 0 1 0 0 0
C5-6 C6-7 C7-T1 T1-2
(1.6%) (3.2%) (3.2%) (3.2%) (1.6%) (0%) (1.6%) (0%) (0%) (0%)
Data represent the count (percentage) of positive tests (defined as severely or moderately hypomobile or hypermobile with pain provocation of 3 or higher on an 11-point numerical rating scale) at each segmental level and side. Control participants were randomly assigned ipsilateral and contralateral arms. LE, lateral epicondylalgia.
RESULTS Analysis was possible using data from 164 patients with LE and 62 controls without LE. Cervical examination was not performed in 1 hearing-impaired patient, due to communication difficulties associated with testing in prone lying. Table 1 provides a summary of the baseline characteristics of the population. The groups were comparable in demographics. Lateral epicondylalgia patients had an average (± SD) duration of injury of 25.1 ± 29.8 weeks (range, 6-25 weeks), with worst pain over the previous week and current resting pain levels (VAS) of 61.9 ± 18.4 mm and 10.8 ± 13.4 mm, respectively. Average pain and disability scores, as measured by the Patient-Rated Tennis Elbow Evaluation, was 39.5 ± 14.1. Spinal manual examination responses for LE and control groups at each site are presented in Table 2. Positive responses were most prevalent in LE patients at C5-6 (18.9%) and C6-7 (17.7%) on the same side as their LE. Comparison of LE and control groups using repeatedmeasures analysis of variance found significant group-bylevel (P = .02) and group-by-side (P = .04) interactions, in the absence of a 3-way interaction. Investigation of the group-by-level interaction (Fig 3) confirmed that positive tests were significantly more common in LE than control patients at C4-5 (P = .01), C5-6 (P = .002), and C6-7 (P = .001) but not at C7-T1 or T1-2 levels (P N .05). Investigation of the group-by-side interaction (Fig 4) showed that positive tests were significantly more common in LE than control patients, more so on the ipsilateral (P = .001) than the contralateral side (P = .02) to the injury. Evaluation of the number of positive palpation sites showed 36% of LE patients had dysfunction of at least 1 spinal palpation site, with 1 subject showing dysfunction
Fig 3. Results of spinal manual examination in LE and control (C) participants at each segmental level. Data illustrate the significant group-by-level interaction. Tests of simple effects showed significant group differences at C4-5 (P = .01), C5-6 (P = .002), and C6-7 (P = .001). at all sites. Linear regression analysis revealed that duration of LE was a significant predictor (unstandardized 0.09; 95% confidence interval, 0.001-0.018; P = .03), whereas worst pain levels (− 0.001, − 0.015 to 0.13; P = .88), age (0.001, − 0.03 to 0.03; P = .93), or sex (0.29, − 0.22 to 0.81; P = .27) were not associated with the total number of positive palpation sites. Patients with more chronic symptoms showed dysfunction at a greater number of sites than those with more acute symptoms. A positive ULNT was found in 41% of LE patients. Logistic regression found severity of elbow pain experienced at rest (odds ratio, 1.03; 95% confidence interval, 1.001-1.06; P = .04) and the number of positive palpation sites (1.25, 1.01-1.55; P = .04) were significant predictors, whereas worst pain level (1.01, 0..99-1.03; P = .27), duration (1.00, 0.991.01; P = .65), age (0.97, 0.93-1.01; P = .09), and sex (0.98, 0.50-1.94; P = .96) were not associated with neurodynamic response. Patients with higher resting elbow pain and dysfunction at multiple cervical or thoracic spinal levels were more likely to have a positive ULNT.
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Fig 4. Results of spinal manual examination in LE and control (C) participants at the side ipsilateral and contralateral to the affected or “matched affected” elbow. Data illustrate the significant group-by-side interaction. Tests of simple effects showed significant group differences for both ipsilateral (P = .001) and contralateral (P = .02) sides.
DISCUSSION The results of this study indicate that cervical spine dysfunction, as determined by pain of 3 or more on an 11point numerical rating scale with severe or moderate hypomobility or hypermobility on manual palpation, exists in LE patients who do not have additional neck or upper limb pain. Dysfunction was evident bilaterally at the cervical spine in unilateral LE and localized to the lower cervical spine (C4-7) but not the thoracic spine. A longer duration of LE symptoms was associated with a greater cervical spine dysfunction. Radial nerve mechanosensitivity, as defined by reproduction of LE symptoms during ULNT and changed by sensitization maneuver, was associated with higher severity of elbow pain at rest and more widespread cervical dysfunction, as inferred by a greater number of positive sites of palpation. Within our LE population with mean duration of 25 weeks, a subgroup of patients displayed dysfunction of at least 1 spinal palpation site (36%) or had a positive ULNT (41%). Results are similar to that found by Waugh (2004), in a study of 81 patients with unilateral LE (mean duration, 31 weeks), excluding those with concurrent upper quadrant symptoms not directly related to their LE. 11 Symptomatic cervical signs, defined as at least 1 active and passive accessory movement (C4-T1) provoking pain and displaying abnormal end feel, were found in 56% of cases, whereas 41% had a positive ULNT that reproduced their LE symptoms. However, much larger rates were found by Berglund et al 4 in their study of 31 patients with lateral elbow pain, where most patients (70%) indicated pain in the cervical or thoracic region on a pain drawing, and 55% experienced pain (either locally or referred to the elbow) on compression of the cervical vertebral foramina. Positive radial nerve neurodynamic tests were found in 58% of patients, defined as pain in the forearm at less than 40° of shoulder abduction. These differences are likely explained
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by differences in measurements as well as their more chronic population (mean, 36 months). Moreover, they recruited patients with lateral elbow pain, rather than a clinical diagnosis of LE, and their study sample included cases in which elbow pain was reproduced by cervical examination, arguably a differential diagnosis for LE. Although causation cannot be inferred from our crosssectional study and the size of the associations detected on regression analyses were small, the data lend some support to the notion that more widespread cervical dysfunction is associated with chronicity. A weak but significant correlation was found between cervical and neurodynamic assessments, indicating that although related, they may reflect different underlying mechanisms. Positive ULNT was similar in both acute and chronic LE but was associated with greater resting pain levels. Previous study of chronic LE did not find an association between positive ULNT and central hyperexcitability as measured by nociceptive withdrawal reflex. 25 Others have found mechanical pain hypersensitivity to be specific to peripheral nerve trunks in patients with LE or carpal tunnel syndrome, with pressure pain thresholds correlated with both pain intensity and duration of symptoms. 26 The mechanisms linking cervical dysfunction and LE remain elusive. We propose that our findings of cervical dysfunction in a subgroup of LE patients without concomitant neck or other arm conditions is consistent with the growing body of evidence inferring central sensitization mechanisms, 24,25,27,28 whereby repeated nociceptor inputs from elbow structures may trigger an increase in the excitability and synaptic efficacy of neurons in central nociceptive pathways. 29 Convergence of afferent input from the lateral elbow and C4-7 cervical segments may underlie the greater incidence of dysfunction at these spinal segments, whereas receptive field expansion may explain the presence of bilateral dysfunction in a unilateral condition. Our proposal is strengthened by the careful history taking and physical examination used to exclude clinically apparent radiculopathy or somatic referral from cervical structures. However, subclinical cases cannot be definitively excluded. An alternative explanation to that of a central sensitization mechanism for the presence of cervical dysfunction might be one of altered mechanical loading of neck during upper limb activities. This alternate explanation is in part supported by reports of generalized motor dysfunction of the upper limb. 23,30,31 The findings from this study may be used to support clinical decision making regarding use of physical modalities for LE. It is recommended that manual examination of the cervical spine and neurodynamic tests be undertaken in the routine assessment of a patient with LE. However, it should be recognized that as standalone clinical tests, they provide only marginal value in the diagnosis of LE, although may help rule out more sinister phenomenon, such as radiculopathy. 32 Preliminary work
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has demonstrated the effectiveness of manual therapy directed to the cervical spine in conjunction with elbow treatment for patients with LE exhibiting cervical dysfunction. 10 Our results highlight patients with longer duration of LE as potential candidates for spinal manual therapy and may explain the greater hypoalgesic effect of cervical compared with thoracic spinal manipulation in this population. 33 Second, results suggest that manual techniques directed to the neural structures through positioning and movement of multiple joints may be of benefit, particularly in patients with more severe resting pain. Although the clinical efficacy of neurodynamic techniques have not been addressed in LE, clinically relevant benefits have been demonstrated in patients with nerve-related neck and arm pain, 34 thumb carpometacarpal osteoarthritis, 35,36 and carpal tunnel syndrome. 37
LIMITATIONS Before drawing clinical implications from this study, it is important to consider several points. First, the population studied was self-referred via community media announcements as a part of a randomized controlled trial and underwent a thorough interview and clinical examination. The examination sought to exclude other comorbid upper limb or cervical symptoms in the experimental sample. This needs to be considered in translation of the findings into clinical practice, that is, the findings relate to a reasonably localized lateral elbow and dorsal forearm pain state and, as such, might represent a more conservative estimate of cervical dysfunction than the general population. Second, we chose measures that are commonly used in clinical assessment of the upper quarter. However, more confidence in the utility, relevance, and importance of these techniques would have been achieved if the examination was performed by an investigator blinded to the group or side studied and if the reliability of the measures had been established in this population. A previous systematic review questioned the reliability of manual tests alone to detect cervical spine dysfunction. 17 However, most studies included in this review examined either segmental mobility or pain as an outcome. In comparison, our study, along with that by Waugh et al, 11 defined spinal segments as impaired if they exhibited abnormal motion and provoked pain. In addition, we examined multiple segmental levels, in an effort to highlight both the segmental location and extent of spinal dysfunction. Furthermore, although there is insufficient evidence in the literature to support an isolated test of the radial nerve, we aimed to identify patients in whom LE symptoms were at least partly related to the nerves in the neck and arm that had become sensitive to movement. We defined a positive ULNT as reproduction of a patient's LE symptoms and changed by structural differentiation (sensitization maneuvers), as recommended in a recent review of the validity of ULNT. 21 Consequently, the test was not performed in control participants, as they did not experience
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such symptoms. Moreover, previous studies have found a high rate of false-positive tests in asymptomatic individuals and recommended that reproduction of the patient's symptoms should be an integral part of the diagnostic criteria. 38
FUTURE STUDIES Despite growing recognition of a relationship between the cervical spine and LE, much needs to be done in this area to better understand the mechanisms linking the 2 and determine its influence on prognosis. There is a need for more detailed and universally agreed classification systems for pain, which presents over the lateral elbow, taking into account that a continuum of concomitant cervical spine pathology may exist. This is particularly relevant for nonspecific arm pain, in which symptoms may be less clear cut and in which diagnosis is essentially made by exclusion. 39 Future studies of LE should consider quantification of neck symptoms using a validated questionnaire, such the Neck Disability Index. 40 Lastly, it is essential that future efforts are made to improve the reliability of measures of cervical and neurodynamic dysfunction so that subgroups can be determined with improved veracity.
CONCLUSION Cervical dysfunction is evident in individuals with LE without obvious neck pain and may reflect central sensitization mechanisms. Further study of the nature of the relationship between cervical dysfunction and LE is required.
Practical Applications • In patients with unilateral lateral epicondylalgia without concomitant cervical or upper limb symptoms, cervical impairment is reasonably common (36%) on manual examination. • Impairment was prevalent bilaterally at C4-7 compared with healthy controls, and duration of injury was associated with greater impairment. • Treatment using manual therapy may be important in preventing chronicity.
FUNDING SOURCES AND POTENTIAL CONFLICTS OF INTEREST This trial was supported by the Australian National Health and Medical Research Council grant 511238
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awarded to Drs Bisset and Vicenzino. Coombes was a recipient of a University of Queensland Research Scholarship. No conflicts of interest were reported for this study.
CONTRIBUTORSHIP INFORMATION Concept development (provided idea for the research): BKC, LB, BV Design (planned the methods to generate the results): BKC, LB, BV Supervision (provided oversight, responsible for organization and implementation, writing of the manuscript): LB, BV Data collection/processing (responsible for experiments, patient management, organization, or reporting data): BKC, BV Analysis/interpretation (responsible for statistical analysis, evaluation, and presentation of the results): BKC, LB, BV Literature search (performed the literature search): BKC, LB, BV Writing (responsible for writing a substantive part of the manuscript): BKC, LB, BV Critical review (revised manuscript for intellectual content, this does not relate to spelling and grammar checking): BKC, LB, BV
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34. Nee RJ, Vicenzino B, Jull GA, Cleland JA, Coppieters MW. Neural tissue management provides immediate clinically relevant benefits without harmful effects for patients with nerve-related neck and arm pain: a randomised trial. J Physiother 2012;58:23-31 [PubMed PMID: 22341379]. 35. Villafane JH, Silva GB, Bishop MD, Fernandez-Carnero J. Radial nerve mobilization decreases pain sensitivity and improves motor performance in patients with thumb carpometacarpal osteoarthritis: a randomized controlled trial. Arch Phys Med Rehabil 2012;93:396-403 [PubMed PMID: 22218138]. 36. Villafane JH, Silva GB, Fernandez-Carnero J. Short-term effects of neurodynamic mobilization in 15 patients with secondary thumb carpometacarpal osteoarthritis. J Manipulative Physiol Ther 2011;34:449-56 [PubMed PMID: 21875519]. 37. De-la-Llave-Rincon AI, Ortega-Santiago R, Ambite-Quesada S, Gil-Crujera A, Puentedura EJ, Valenza MC, et al. Response of pain intensity to soft tissue mobilization and neurodynamic technique: a series of 18 patients with chronic carpal tunnel syndrome. J Manipulative Physiol Ther 2012;35:420-7 [PubMed PMID: 22858234]. 38. Davis DS, Anderson IB, Carson MG, Elkins CL, Stuckey LB. Upper limb neural tension and seated slump tests: the false positive rate among healthy young adults without cervical or lumbar symptoms. J Man Manip Ther 2008;16:136-41 [PubMed PMID: 19119402]. 39. Helliwell PS, Bennett RM, Littlejohn G, Muirden KD, Wigley RD. Towards epidemiological criteria for soft-tissue disorders of the arm. Occup Med 2003;53:313-9 [PubMed PMID: 12890830]. 40. Vernon H. The Neck Disability Index: state-of-the-art, 19912008. J Manipulative Physiol Ther 2008;31:491-502 [PubMed PMID: 18803999].
ABSTRACT Objective: The purposes of this study were to examine the prevalence and distribution of spinal and neurodynamic dysfunction in a population with unilateral lateral epicondylalgia (LE) without concomitant cervical or upper limb symptoms, compare with cervical examination in a healthy control population, and investigate potential associations with clinical and demographic factors. Methods: This cross-sectional study included 165 patients with LE along with 62 healthy controls. Manual examination (C4-T2) was performed by an unblinded examiner with dysfunction defined as pain of 3 or higher on a numerical rating scale in the presence of a severe or moderate hypomobility or hypermobility. Neurodynamic testing (radial nerve) was classified positive if LE symptoms were reproduced and altered by sensitization maneuver. Repeated-measures analysis of variance was used to compare sides, segmental levels, and groups. Regression analysis was used to determine associations between variables. Results: Thirty-six percent of patients had dysfunction of at least 1 spinal palpation site, and 41% had a positive neurodynamic test. Significant group-by-level (P = .02) and group-by-side (P = .04) interactions were found for spinal examination, with greater dysfunction bilaterally at C4-7 (P b .01) in LE compared with control arms. The number of positive palpation sites was associated with injury duration (P = .03), whereas neurodynamic response was associated with severity of resting pain (P = .04). Conclusions: Cervical dysfunction is evident in individuals with LE without obvious neck pain and may reflect central sensitization mechanisms. Further study of the nature of the relationship between cervical dysfunction and LE is required. (J Manipulative Physiol Ther 2014;37:79-86) Key Indexing Terms: Tennis Elbow; Neck Pain; Radial Nerve; Musculoskeletal Manipulations
ateral epicondylalgia (LE), also known as tennis elbow, is empirically considered a tendinopathy of the extensor carpi radialis brevis origin. 1 However, there is also recognition of a relationship between the cervical spine, radial nerve, and LE. 2,3 First, there are findings of a greater prevalence of neck pain in patients with lateral elbow pain compared with an age-matched control population 4 as well as greater radial nerve
L a
Researcher, School of Health and Rehabilitation Sciences, University of Queensland, St Lucia, Queensland, Australia. b Researcher, Griffith Health Institute, Griffith University, Gold Coast, Queensland, Australia. Submit requests for reprints to: Bill Vicenzino, PhD, Therapies Building 84A, University of Queensland, St Lucia 4072, Queensland, Australia (e-mail: [email protected]). Paper submitted July 16, 2013; in revised form September 12, 2013; accepted September 20, 2013. 0161-4754/$36.00 Copyright © 2014 by National University of Health Sciences. http://dx.doi.org/10.1016/j.jmpt.2013.12.005
mechanosensitivity of the affected arm in patients with unilateral symptoms. 3,5 Others have found widespread pain over the neck or upper limb to commonly coexist alongside chronic epicondylitis, with widespread symptoms being associated with chronicity. 6 Secondly, poorer long-term prognosis is predicted by self-reported neck pain, independent of high baseline lateral elbow pain intensity. 7 Juxtaposed upon this is evidence of the effectiveness of manual therapy directed toward the cervicothoracic spine in conjunction with elbow treatment, including benefit in previously recalcitrant cases, 8 fewer treatment sessions, 9 and greater improvement in short-term pain. 10 However, only the latter pilot study of 10 participants was a randomized trial, highlighting that more research in this area is needed. With estimates ranging from 57% to 90%, 4,11,12 the true prevalence of related cervical spine and radial nerve pathology in the LE population has not been conclusively established. Differences in eligibility criteria, examination procedure, and criteria used to detect dysfunction provide 79
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Fig 1. Flow chart for selection of LE and control participants. Data for the LE group were collected before enrollment into a randomized controlled trial, 13 the methodology for which is described in detail elsewhere. 14
strong sources of heterogeneity between studies. Moreover, the presence of cervical dysfunction may be seen as a differential diagnosis from true LE 2 or as a subgroup thereof. The extent and distribution of spinal and neurodynamic dysfunction in LE individuals without concomitant neck or other upper limb symptoms have not been previously evaluated and provide a logical step for this field of interest. This study aimed to evaluate whether there are differences in manual examination of the cervical and thoracic spine between LE patients and healthy controls who did not have additional (or concomitant) neck or upper limb symptoms. Second, the relationships between spinal manual examination, radial nerve neurodynamic test responses and pain severity, duration of injury, age, and sex were studied to further shed light on potential mechanisms.
METHODS Design This cross-sectional, comparative study investigated the prevalence of abnormal findings from a clinical examination of the cervical and thoracic spine and radial nerve in individuals with and without unilateral LE (Fig 1). Data for the LE group were collected before enrollment into a randomized controlled trial, 13 the methodology for which is described in detail elsewhere. 14
Participants All patients were recruited from the greater Brisbane region of Australia through community media advertisements. Eligibility was determined by a 2-stage process (telephone interview and physical examination) by 1 researcher (BKC) and confirmed by a second researcher (BV). 14 One hundred sixty-five patients with a clinical diagnosis of LE, meeting the following criteria, were included: unilateral elbow pain over the lateral epicondyle for longer than 6 weeks and pain provoked by at least 2 of the following: gripping, palpation, resisted wrist or middle finger extension, or stretching of forearm extensor muscles with reduced pain-free grip. Exclusion criteria were recent injection or physiotherapy, neck or other upper limb symptoms necessitating treatment or preventing participation in usual work or recreational activities in the preceding 6 months, exacerbation of elbow pain with neck examination (ie, active and passive motion, palpation), sensory disturbance of the hands, fractures, elbow surgery, malignancy or inflammatory disorders, pregnancy, breastfeeding, or contraindication to injection. Sixty-two healthy control participants aged 35 to 70 years were included. Exclusion criteria for control participants were history of LE and neck or other upper limb symptoms necessitating treatment or preventing participation in usual work or recreational activities in the preceding 6 months. Ethical approval was granted by the
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institutional review board (University of Queensland), and informed written consent was obtained from all patients. This trial was supported by the Australian National Health and Medical Research Council grant 511238. Coombes was in receipt of a University of Queensland Research Scholarship.
Outcome measures The tests used in this study were selected because of their frequent use in clinical assessment of the neck and upper limb. All testing was completed by a single physiotherapist (BKC) with a postgraduate degree in musculoskeletal physiotherapy who was not blinded to whether the subject had LE. Spinal manual examination was performed on all patients, whereas neurodynamic function was evaluated in LE patients only. Patients were asked to rate the level of elbow pain currently experienced at rest and the worst level of pain experienced during the past week on 100-mm visual analog scales (VAS) with the following end points: no pain (0 mm) and worst pain imaginable pain (100 mm). Manual Examination. Intersegmental manual examination or passive motion palpation of the cervical and thoracic spine was performed between C4 and T2 segments bilaterally on all patients in prone lying. The examiner rated the intersegmental end feel on a previously defined scale, 15 ranging from 1 (severe hypomobility) to 7 (severe hypermobility), with 4 representing normal mobility. Previous study of the reliability of this method in participants with cervicogenic headache or migraine and a control group reported high κ values. 15 The participant also verbally rated any pain provoked by examination on an 11point numerical rating scale. A positive response was recorded at each of the 10 sites (5 levels × 2 sides) based on the following criteria: moderate to severe hypomobility or hypermobility (ie, scores of 1.2 and 6.7, respectively) along with a pain response of 3 or greater. 15 An aggregate score (range, 0-10), consisting of the sum of positive palpation sites, was also derived for further analyses. We based the criteria for dysfunction on assessment of both the quality of passive segmental motion as well as provocation of pain, due to the qualitative nature of assessment of joint motion alone. 16-18 Previous review of the reliability of static spinal palpation found that acceptable κ values were more common for studies evaluating pain provocation, although no one method could be deemed clearly superior. 19 Neurodynamic Examination. The upper limb neurodynamic test (ULNT) for the radial nerve was performed as previously described, 20 using the following sequencing: shoulder girdle depression, elbow extension, shoulder internal rotation, pronation, wrist and finger flexion, and shoulder abduction to the end of range or until symptoms were produced (Fig 2). Once such a sensation was provoked, structural differentiation between neurogenic and nonneurogenic sources of pain was performed by the addition of sensitizing move-
Fig 2. Upper limb neurodynamic test with radial nerve bias, comprising shoulder girdle depression, elbow extension, shoulder internal rotation, pronation, wrist and finger flexion, and shoulder abduction, followed by sensitizing movements of shoulder girdle elevation or cervical lateral flexion. (Color version of figure is available online.)
ments at a site distant to the pain (shoulder girdle elevation or cervical lateral flexion) while all other test components were maintained. Based on a previous study evaluating the validity of the ULNT, 21 the test was considered positive if the following 2 criteria were present: (1) the subject's symptoms were reproduced at least partially, and (2) symptoms were altered by structural differentiation. Moderate reliability (κ = 0.44) has been reported for the radial nerve ULNT using the above criteria. 22
Data Analysis This study was powered to detect differences between LE and control participants based on measures not evaluated in this study, including quantitative sensory testing, anxiety, and depression, the results of which are published elsewhere. 23,24 Statistical analysis was performed using SPSS 20 (IBM, Somers, NY), with a P b .05 significance level. Manual examination of the cervical and thoracic spine was compared between LE and control groups using repeated-measures analysis of variance, including the within-subject factors of side (ipsilateral or contralateral) and level (C4-5, C5-6, C6-7, C7-T1, or T1-2) and the covariates age and sex. Control patients were randomly allocated a “matched” affected arm, referred to herein as the ipsilateral arm, such that the control group had an equivalent proportion of dominant-sided arms as that observed in the LE group to account for any potential influence of hand dominance. Linear regression was used to evaluate potential associations of severity of pain, age, sex, and duration on the aggregate score of manual examination, that is, the sum
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Table 1. Baseline characteristics of LE and control participants LE (n = 164) Controls (n = 62) Age (y) Female Body mass index Manual occupation Sport involving strong gripping Duration of symptoms (wk) Incident cases Dominant arm affected Worst pain (VAS: 0-100) Current resting pain (VAS: 0-100) Pain and disability (PRTEE: 0-100) Pain-free grip (N)
49.6 ± 9.0 63 (38.4%) 26.5 ± 5.1 41 (24.8%) 58 (35.2%) 25.1 ± 29.8 125 (76.2%) 116 (70.7%) 61.9 ± 18.4 10.8 ± 13.4 39.5 ± 14.1 150.7 ± 128.4
49.6 ± 8.7 28 (45.2%) 25.4 ± 4.7 12 (19.4%) 14 (22.6%)
Data represent mean ± SD or count (percentage). LE, lateral epicondylalgia; VAS, visual analog scale.
of positive spinal palpation sites. Logistic regression was used to evaluate the relationship of these factors on the ULNT response. All variables were simultaneously entered into each model.
Table 2. Results of spinal manual examination in LE and control patients Segmental level
Side
LE (n = 164)
Controls (n = 62)
C4-5
Ipsilateral Contralateral Ipsilateral Contralateral Ipsilateral Contralateral Ipsilateral Contralateral Ipsilateral Contralateral
19 (11.6%) 17 (10.4%) 31 (18.9%) 18 (11.0%) 29 (17.7%) 8 (4.9%) 8 (4.9%) 4 (2.4%) 4 (2.4%) 2 (1.2%)
1 2 2 2 1 0 1 0 0 0
C5-6 C6-7 C7-T1 T1-2
(1.6%) (3.2%) (3.2%) (3.2%) (1.6%) (0%) (1.6%) (0%) (0%) (0%)
Data represent the count (percentage) of positive tests (defined as severely or moderately hypomobile or hypermobile with pain provocation of 3 or higher on an 11-point numerical rating scale) at each segmental level and side. Control participants were randomly assigned ipsilateral and contralateral arms. LE, lateral epicondylalgia.
RESULTS Analysis was possible using data from 164 patients with LE and 62 controls without LE. Cervical examination was not performed in 1 hearing-impaired patient, due to communication difficulties associated with testing in prone lying. Table 1 provides a summary of the baseline characteristics of the population. The groups were comparable in demographics. Lateral epicondylalgia patients had an average (± SD) duration of injury of 25.1 ± 29.8 weeks (range, 6-25 weeks), with worst pain over the previous week and current resting pain levels (VAS) of 61.9 ± 18.4 mm and 10.8 ± 13.4 mm, respectively. Average pain and disability scores, as measured by the Patient-Rated Tennis Elbow Evaluation, was 39.5 ± 14.1. Spinal manual examination responses for LE and control groups at each site are presented in Table 2. Positive responses were most prevalent in LE patients at C5-6 (18.9%) and C6-7 (17.7%) on the same side as their LE. Comparison of LE and control groups using repeatedmeasures analysis of variance found significant group-bylevel (P = .02) and group-by-side (P = .04) interactions, in the absence of a 3-way interaction. Investigation of the group-by-level interaction (Fig 3) confirmed that positive tests were significantly more common in LE than control patients at C4-5 (P = .01), C5-6 (P = .002), and C6-7 (P = .001) but not at C7-T1 or T1-2 levels (P N .05). Investigation of the group-by-side interaction (Fig 4) showed that positive tests were significantly more common in LE than control patients, more so on the ipsilateral (P = .001) than the contralateral side (P = .02) to the injury. Evaluation of the number of positive palpation sites showed 36% of LE patients had dysfunction of at least 1 spinal palpation site, with 1 subject showing dysfunction
Fig 3. Results of spinal manual examination in LE and control (C) participants at each segmental level. Data illustrate the significant group-by-level interaction. Tests of simple effects showed significant group differences at C4-5 (P = .01), C5-6 (P = .002), and C6-7 (P = .001). at all sites. Linear regression analysis revealed that duration of LE was a significant predictor (unstandardized 0.09; 95% confidence interval, 0.001-0.018; P = .03), whereas worst pain levels (− 0.001, − 0.015 to 0.13; P = .88), age (0.001, − 0.03 to 0.03; P = .93), or sex (0.29, − 0.22 to 0.81; P = .27) were not associated with the total number of positive palpation sites. Patients with more chronic symptoms showed dysfunction at a greater number of sites than those with more acute symptoms. A positive ULNT was found in 41% of LE patients. Logistic regression found severity of elbow pain experienced at rest (odds ratio, 1.03; 95% confidence interval, 1.001-1.06; P = .04) and the number of positive palpation sites (1.25, 1.01-1.55; P = .04) were significant predictors, whereas worst pain level (1.01, 0..99-1.03; P = .27), duration (1.00, 0.991.01; P = .65), age (0.97, 0.93-1.01; P = .09), and sex (0.98, 0.50-1.94; P = .96) were not associated with neurodynamic response. Patients with higher resting elbow pain and dysfunction at multiple cervical or thoracic spinal levels were more likely to have a positive ULNT.
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Fig 4. Results of spinal manual examination in LE and control (C) participants at the side ipsilateral and contralateral to the affected or “matched affected” elbow. Data illustrate the significant group-by-side interaction. Tests of simple effects showed significant group differences for both ipsilateral (P = .001) and contralateral (P = .02) sides.
DISCUSSION The results of this study indicate that cervical spine dysfunction, as determined by pain of 3 or more on an 11point numerical rating scale with severe or moderate hypomobility or hypermobility on manual palpation, exists in LE patients who do not have additional neck or upper limb pain. Dysfunction was evident bilaterally at the cervical spine in unilateral LE and localized to the lower cervical spine (C4-7) but not the thoracic spine. A longer duration of LE symptoms was associated with a greater cervical spine dysfunction. Radial nerve mechanosensitivity, as defined by reproduction of LE symptoms during ULNT and changed by sensitization maneuver, was associated with higher severity of elbow pain at rest and more widespread cervical dysfunction, as inferred by a greater number of positive sites of palpation. Within our LE population with mean duration of 25 weeks, a subgroup of patients displayed dysfunction of at least 1 spinal palpation site (36%) or had a positive ULNT (41%). Results are similar to that found by Waugh (2004), in a study of 81 patients with unilateral LE (mean duration, 31 weeks), excluding those with concurrent upper quadrant symptoms not directly related to their LE. 11 Symptomatic cervical signs, defined as at least 1 active and passive accessory movement (C4-T1) provoking pain and displaying abnormal end feel, were found in 56% of cases, whereas 41% had a positive ULNT that reproduced their LE symptoms. However, much larger rates were found by Berglund et al 4 in their study of 31 patients with lateral elbow pain, where most patients (70%) indicated pain in the cervical or thoracic region on a pain drawing, and 55% experienced pain (either locally or referred to the elbow) on compression of the cervical vertebral foramina. Positive radial nerve neurodynamic tests were found in 58% of patients, defined as pain in the forearm at less than 40° of shoulder abduction. These differences are likely explained
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by differences in measurements as well as their more chronic population (mean, 36 months). Moreover, they recruited patients with lateral elbow pain, rather than a clinical diagnosis of LE, and their study sample included cases in which elbow pain was reproduced by cervical examination, arguably a differential diagnosis for LE. Although causation cannot be inferred from our crosssectional study and the size of the associations detected on regression analyses were small, the data lend some support to the notion that more widespread cervical dysfunction is associated with chronicity. A weak but significant correlation was found between cervical and neurodynamic assessments, indicating that although related, they may reflect different underlying mechanisms. Positive ULNT was similar in both acute and chronic LE but was associated with greater resting pain levels. Previous study of chronic LE did not find an association between positive ULNT and central hyperexcitability as measured by nociceptive withdrawal reflex. 25 Others have found mechanical pain hypersensitivity to be specific to peripheral nerve trunks in patients with LE or carpal tunnel syndrome, with pressure pain thresholds correlated with both pain intensity and duration of symptoms. 26 The mechanisms linking cervical dysfunction and LE remain elusive. We propose that our findings of cervical dysfunction in a subgroup of LE patients without concomitant neck or other arm conditions is consistent with the growing body of evidence inferring central sensitization mechanisms, 24,25,27,28 whereby repeated nociceptor inputs from elbow structures may trigger an increase in the excitability and synaptic efficacy of neurons in central nociceptive pathways. 29 Convergence of afferent input from the lateral elbow and C4-7 cervical segments may underlie the greater incidence of dysfunction at these spinal segments, whereas receptive field expansion may explain the presence of bilateral dysfunction in a unilateral condition. Our proposal is strengthened by the careful history taking and physical examination used to exclude clinically apparent radiculopathy or somatic referral from cervical structures. However, subclinical cases cannot be definitively excluded. An alternative explanation to that of a central sensitization mechanism for the presence of cervical dysfunction might be one of altered mechanical loading of neck during upper limb activities. This alternate explanation is in part supported by reports of generalized motor dysfunction of the upper limb. 23,30,31 The findings from this study may be used to support clinical decision making regarding use of physical modalities for LE. It is recommended that manual examination of the cervical spine and neurodynamic tests be undertaken in the routine assessment of a patient with LE. However, it should be recognized that as standalone clinical tests, they provide only marginal value in the diagnosis of LE, although may help rule out more sinister phenomenon, such as radiculopathy. 32 Preliminary work
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has demonstrated the effectiveness of manual therapy directed to the cervical spine in conjunction with elbow treatment for patients with LE exhibiting cervical dysfunction. 10 Our results highlight patients with longer duration of LE as potential candidates for spinal manual therapy and may explain the greater hypoalgesic effect of cervical compared with thoracic spinal manipulation in this population. 33 Second, results suggest that manual techniques directed to the neural structures through positioning and movement of multiple joints may be of benefit, particularly in patients with more severe resting pain. Although the clinical efficacy of neurodynamic techniques have not been addressed in LE, clinically relevant benefits have been demonstrated in patients with nerve-related neck and arm pain, 34 thumb carpometacarpal osteoarthritis, 35,36 and carpal tunnel syndrome. 37
LIMITATIONS Before drawing clinical implications from this study, it is important to consider several points. First, the population studied was self-referred via community media announcements as a part of a randomized controlled trial and underwent a thorough interview and clinical examination. The examination sought to exclude other comorbid upper limb or cervical symptoms in the experimental sample. This needs to be considered in translation of the findings into clinical practice, that is, the findings relate to a reasonably localized lateral elbow and dorsal forearm pain state and, as such, might represent a more conservative estimate of cervical dysfunction than the general population. Second, we chose measures that are commonly used in clinical assessment of the upper quarter. However, more confidence in the utility, relevance, and importance of these techniques would have been achieved if the examination was performed by an investigator blinded to the group or side studied and if the reliability of the measures had been established in this population. A previous systematic review questioned the reliability of manual tests alone to detect cervical spine dysfunction. 17 However, most studies included in this review examined either segmental mobility or pain as an outcome. In comparison, our study, along with that by Waugh et al, 11 defined spinal segments as impaired if they exhibited abnormal motion and provoked pain. In addition, we examined multiple segmental levels, in an effort to highlight both the segmental location and extent of spinal dysfunction. Furthermore, although there is insufficient evidence in the literature to support an isolated test of the radial nerve, we aimed to identify patients in whom LE symptoms were at least partly related to the nerves in the neck and arm that had become sensitive to movement. We defined a positive ULNT as reproduction of a patient's LE symptoms and changed by structural differentiation (sensitization maneuvers), as recommended in a recent review of the validity of ULNT. 21 Consequently, the test was not performed in control participants, as they did not experience
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such symptoms. Moreover, previous studies have found a high rate of false-positive tests in asymptomatic individuals and recommended that reproduction of the patient's symptoms should be an integral part of the diagnostic criteria. 38
FUTURE STUDIES Despite growing recognition of a relationship between the cervical spine and LE, much needs to be done in this area to better understand the mechanisms linking the 2 and determine its influence on prognosis. There is a need for more detailed and universally agreed classification systems for pain, which presents over the lateral elbow, taking into account that a continuum of concomitant cervical spine pathology may exist. This is particularly relevant for nonspecific arm pain, in which symptoms may be less clear cut and in which diagnosis is essentially made by exclusion. 39 Future studies of LE should consider quantification of neck symptoms using a validated questionnaire, such the Neck Disability Index. 40 Lastly, it is essential that future efforts are made to improve the reliability of measures of cervical and neurodynamic dysfunction so that subgroups can be determined with improved veracity.
CONCLUSION Cervical dysfunction is evident in individuals with LE without obvious neck pain and may reflect central sensitization mechanisms. Further study of the nature of the relationship between cervical dysfunction and LE is required.
Practical Applications • In patients with unilateral lateral epicondylalgia without concomitant cervical or upper limb symptoms, cervical impairment is reasonably common (36%) on manual examination. • Impairment was prevalent bilaterally at C4-7 compared with healthy controls, and duration of injury was associated with greater impairment. • Treatment using manual therapy may be important in preventing chronicity.
FUNDING SOURCES AND POTENTIAL CONFLICTS OF INTEREST This trial was supported by the Australian National Health and Medical Research Council grant 511238
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awarded to Drs Bisset and Vicenzino. Coombes was a recipient of a University of Queensland Research Scholarship. No conflicts of interest were reported for this study.
CONTRIBUTORSHIP INFORMATION Concept development (provided idea for the research): BKC, LB, BV Design (planned the methods to generate the results): BKC, LB, BV Supervision (provided oversight, responsible for organization and implementation, writing of the manuscript): LB, BV Data collection/processing (responsible for experiments, patient management, organization, or reporting data): BKC, BV Analysis/interpretation (responsible for statistical analysis, evaluation, and presentation of the results): BKC, LB, BV Literature search (performed the literature search): BKC, LB, BV Writing (responsible for writing a substantive part of the manuscript): BKC, LB, BV Critical review (revised manuscript for intellectual content, this does not relate to spelling and grammar checking): BKC, LB, BV
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