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BJSM Online First, published on October 21, 2013 as 10.1136/bjsports-2013-092535
Review

Sensory and motor decits exist on the non-injured


side of patients with unilateral tendon pain and
disabilityimplications for central nervous system
involvement: a systematic review with meta-analysis
L J Heales,1 E C W Lim,1,2 P W Hodges,1 B Vicenzino1

Additional material is ABSTRACT an animal model of unilateral tendinopathy have


published online only. To view Introduction Tendinopathy manifests as activity- conrmed local signs including; degenerative
please visit the journal online
(http://dx.doi.org/10.1136/
related tendon pain with associated motor and sensory changes, neovascularisation8 and changes in the
bjsports-2013-092535) impairments. Tendon tissue changes in animals present mechanical properties of the tissue including
1 in injured as well as contralateral non-injured tendon. decreased elasticity and maximum stress at failure.9
The University of Queensland,
NHMRC Centre of Clinical This review investigated evidence for bilateral sensory This diverse array of changes is likely to affect the
Research Excellence in Spinal and motor system involvement in unilateral tendinopathy sensory and motor systems, yet there is limited
Pain, Injury and Health, School in humans. understanding of how they are related.
of Health and Rehabilitation Methods A comprehensive search of electronic An interesting and paradigm challenging observa-
Sciences, Division of
Physiotherapy, Brisbane,
databases, and reference lists using keywords relating to tion from an animal model of repetitive unilateral
Queensland, Australia bilateral outcomes in unilateral tendinopathy was exercise has been the presence of bilateral tendon
2
Physiotherapy Department, undertaken. Study quality was rated with the changes, that is biological changes in the tendon of
Singapore General Hospital, Epidemiological Appraisal Instrument and meta-analyses the non-exercised limb. This was evidenced by
Singapore, Singapore
carried out where appropriate. Analysis focused on increased inltrating macrophages not only in the
Correspondence to comparison of measures in the non-symptomatic side of tendon of the injured limb but also in the contralat-
Professor Bill Vicenzino, School patients against pain-free controls. eral limb,10 a signicant increase in tenocytes in
of Health & Rehabilitation Results The search revealed 5791 studies, of which 20 both limbs11 and a bilateral increase in vascularity
Sciences, Division of were included (117 detailed reviews, 25 met criteria). of the tendon by week 3. These observations lead
Physiotherapy,
The University of Queensland, There were 17 studies of lateral epicondylalgia (LE) and to speculation of a centrally mediated process in
St Lucia, Brisbane, one each for patellar, Achilles and rotator cuff the pathogenesis of tendinopathy, which underpins
Queensland 4072, Australia; tendinopathy. Studies of LE were available for meta- activity-related pain and disability, but this has
b.vicenzino@uq.edu.au analysis revealing the following weighted pooled mean received limited attention in literature.
Accepted 21 September 2013
decits: pressure pain thresholds (144.3 kPa; 95% CI The biological evidence of bilateral tendon path-
169.2 to 119.2 p<0.001), heat pain thresholds ology in a unilateral exercise-induced tendinopathy
(1.2C; 95% CI 2.1 to 0.2, p<0.001), cold pain underpins the speculation that bilateral changes are
thresholds (3.1C; 95% CI 1.8 to 4.4, p<0.001) and likely to manifest in patients who present with a
reaction time (37.8 ms; 95% CI 24.8 to 50.7, p<0.001). unilateral tendon problem and the pathogenesis of
Discussion Decits in sensory and motor systems this condition may be more complex than is readily
present bilaterally in unilateral tendinopathy. This implies explained by local pathology. This systematic
potential central nervous system involvement. This review aimed to address the issue of motor and
indicates that rehabilitation should consider the sensory system changes associated with
contralateral side of patients. Research of unilateral activity-related pain related to the tendon. To this
tendinopathy needs to consider comparison against pain- end we systematically assessed the literature of
free controls in addition to the contralateral side to gain a human experimentation to ascertain whether
complete understanding of sensory and motor features. changes in the motor or sensory systems occur in
the contralateral side of patients with unilateral
tendinopathy.
INTRODUCTION
Tendinopathy impacts substantially on participation METHODS
in physical activity1 and is characterised clinically, Search strategy
by activity-related pain, focal tenderness on palpa- A comprehensive search of electronic databases
tion and decreased functional capacity of the (MEDLINEvia Ovid, Scopus and PubMed) was
segment (eg, strength and movement).2 undertaken by LH to identify all English language
Historically, tendinopathy has been considered as studies for all years up to May 2013. Keyword,
local degeneration with pathological changes title and abstract information were used. Search
including increased type III collagen bres, an asso- terms were tennis elbow AND bilat* (the symbol
To cite: Heales LJ, ciated increase in ground substance and subsequent is used for identifying all words starting with bilat,
Lim ECW, Hodges PW, et al.
Br J Sports Med Published
loss of hierarchical structure of the tendon.3 4 This eg, bilateral, bilaterally and bilateralism) OR
Online First: [ please include loss of cellular homeostasis5 has been suggested to jumpers knee AND bilat* OR tendin* AND
Day Month Year] contribute to neovasularisation, which has been bilat* OR tendo* AND bilat* OR epicondy*
doi:10.1136/bjsports-2013- variously proposed to relate to features as diverse AND bilat*. A thorough manual search of the ref-
092535 as tendon repair6 and chronic pain.7 Studies using erence lists for all included studies was undertaken

Copyright
Heales LJ, et al. Br JArticle
Sports Medauthor (ordoi:10.1136/bjsports-2013-092535
2013;0:18. their employer) 2013. Produced by BMJ Publishing Group Ltd under licence. 1
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Review

to identify articles that may not be listed on electronic databases, measured any aspect of the sensory system (eg, pressure or tem-
articles without abstracts that may have been missed by the perature pain thresholds and proprioception), physical features
initial search strategy, articles from networks or conferences and of anatomy (eg, wrist angle and structural tendon changes) and
grey literature (ie, theses and books). motor function (eg, reaction time (simple and complex), corti-
comotor excitability, movement, muscle output (eg, grip
Study selection strength)).
Upon retrieval from the above search strategy all titles and
abstracts were scanned by LH to identify studies that included
bilateral measurement in patients with unilateral tendinopathy, Statistical methods
and with a healthy cohort included for comparison. An a priori The reliability of the quality assessment was evaluated using
decision was made that a decit on the side contralateral to the SPSS V.17 software (SPSS Inc, Chicago, Illinois, USA).
symptoms could be conrmed if the measure of sensory or Statistics were used to report the total inter-rater reliability
motor function of the contralateral limb was different to that between the two assessors. Inter-rater reliability was considered
reported for the corresponding limb of control participants. as poor (<0.00), slight (0.000.2), fair (0.210.4), moderate
Presence of bilateral decits could not be determined from com- (0.410.6), substantial (0.610.8) or almost perfect (0.81
parison between sides within a participant with unilateral symp- 1.0).13 Where possible and appropriate the data were pooled
toms as the absence of difference between sides could indicate with formal meta-analytical techniques using RevMan 5
that either (1) no decit was present for either side or, (2) a (Copenhagen, Denmark: The Nordic Cochrane Centre, The
decit was present for both sides. Thus studies without a Cochrane Collaboration, 2006). A meta-analysis was performed
healthy control group for comparison could not be included. using a random effects model to obtain weighted pooled mean
For the purposes of this review, we dened the motor system differences and their 95% CIs. I2 was calculated and used as an
broadly as encompassing bone, joint, tendon and muscle as well indicator of the extent between trial heterogeneity. Differences
as neuromuscular control. The sensory system was dened as in sensory and motor system measures between the side contra-
involving nociceptive and proprioceptive systems, usually mea- lateral to the tendinopathy symptoms in patients and the corre-
sured with quantitative sensory testing. sponding side in pain-free control participants were calculated
All eligible studies were recorded and the full text was such that negative differences indicate that the measure for the
obtained. LH then undertook a detailed evaluation using prede- patient with unilateral tendinopathy represented a decit relative
termined criteria based on study design, clinical diagnosis of to that for the control participants, and positive differences indi-
unilateral tendinopathy and quantitative reports of bilateral mea- cate the opposite. Standardised mean differences (SMD) were
sures. Only data representative of unilateral tendinopathy were calculated where meta-analysis was not possible. SMDs were
included in this review. Studies that included individuals with interpreted as small 0.2, medium 0.5 and large 0.8 effect size.14
both bilateral and unilateral tendinopathies were retained if data
were reported separately for the unilateral cases. Reviews, case RESULTS
studies, letters to the editor and studies of animals were Database search
excluded, along with non-English language publications. The comprehensive search strategy yielded a total of 5791 pub-
lications from electronic databases and manually searched refer-
Quality assessment ence lists. All titles and abstracts were screened and 117
The quality of the included studies was scored using the epi- potentially relevant studies were identied. Of these, 25 satised
demiological appraisal instrument (EAI).12 The EAI was con- the selection criteria and reported bilateral nociceptive, sensory
densed to 26 items. As this review was not focused on clinical and motor measures of participants with unilateral tendinopathy
trials, items related to randomisation, follow-up and environ- contrasted with data for controls (gure 1). Two studies were
mental variables were not applicable and excluded from the excluded as they reported secondary presentation of data pub-
assessment. Prior to the quality evaluation, detailed criteria to lished elsewhere.15 16 Seven authors were contacted during data
determine each response were modied from the original tool extraction to provide additional information for the following
to match the purpose of this review and agreed on by all asses- reasons: data only presented graphically17; affected and
sors. Two independent assessors scored the studies. Any dis- unaffected limb data combined1820; no control data for a spe-
agreements were reviewed by consultation with a third party. cic outcome measure21 and insufcient details for data.22 23
Each item was independently scored using the standardised Three authors supplied data on at least one outcome; one pro-
scale; Yes (score=1), Partial (score=0.5), No (score=0), vided insufcient useable data; and two were unable to be con-
Unable to determine (score=0) or Not applicable (item was tacted. Of the 25 studies that satised the inclusion criteria a
removed from scoring). Studies were given an overall score, total of 20 were included in the review. The composition of
which was derived as an average of the total for all 26 items these per anatomical region included 17 LE, 1 patella tendino-
(range 01). pathy, 1 Achilles tendinopathy and 1 rotator cuff tendinopathy.

Data extraction
LH completed data extraction, with all queries discussed and Study characteristics
resolved by all assessors. Data describing the sample population Studies varied in terms of location, timing and population.
and study methodology as well as the descriptives for the Eight studies (40%) were conducted in Australia, four (20%) in
reported measures of pain, sensory and motor function were Spain, two (10%) in Canada and one (5%) each in the USA, the
extracted for the contralateral side in unilateral tendinopathy UK, Finland, Norway, Sweden and Denmark. One study (5%)
and the corresponding side in controls. If additional informa- was published in the 1980s; two (10%) in 1990s; 11 (55%) in
tion was required authors were contacted. 2000s and six (30%) since 2010. Sample sizes varied widely
Studies were reviewed for measures of pain, sensory and from 1924 to 238 participants.25 In general the number of LE
motor functions. Measures were considered relevant if they participants did not match the number of controls.

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Figure 1 Selection process for inclusion in the review.

Quality assessment Meta-analysis


The overall agreement between the two reviewers was almost Not all studies contributed data to the meta-analysis as many
perfect (=0.897, p<0.01)13 with 484 agreements of 520 deci- were the only study for tendinopathy in a specic anatomical
sions. The results from the quality assessment using the modied location (ie, patella tendinopathy, rotator cuff tendinopathy and
EAI12 demonstrated a median score of 0.46 (range 0.290.63) out Achilles tendinopathy) and there were differences in measure-
of a possible 1 (quality assessment results, web only supplementary ments used, with some reported in only one study (eg, cortico-
le A). Overall the quality assessment revealed only 15% (3 of 20) motor excitability or electrical pain thresholds). The studies that
used diagnostic imaging as part of the eligibility criteria; only 25% could not be included in the meta-analysis are discussed indi-
(5/20) clearly described their study population and how and where vidually in the appraisal section. Only studies of patients with
they recruited participants, and only 20% (4/20) used priori LE could be subjected to meta-analyses. Of these, six studied
sample size calculations. Only 35% (7/20) of the studies described pressure pain threshold at sites other than the elbow, three
their study design and no longitudinal or prospective studies were studied heat pain and cold pain thresholds bilaterally, and two
identied. The two reviewers were unable to determine if any studied reaction time and speed of movement bilaterally.
study blinded the participants to the outcome measures and only The weighted pooled mean difference demonstrated that pres-
15% (3/20) of studies blinded the assessors to the participants sure pain thresholds were 144.3 kPa (95% CI 119.2 to 169.2,
condition during the experiments. Despite the importance of I2=46%) lower in the participants limb that was contralateral to
using validated measures only 5% (1/20) of the studies reported the unilateral LE symptoms than the corresponding side of con-
the validity of their main measures. No studies included prior trols (p<0.001; gure 2). Heat pain thresholds were 1.2C (95%
history of the condition in the analysis, 20% (4/20) adjusted for CI 0.2 to 2.1, I2=33%) lower and cold pain thresholds were 3.1C
individual covariates and confounders, 10% (2/20) reported the (95% CI 1.8 to 4.4, I2=0%) higher on the contralateral side of
results by severity of the condition and 15% (3/20) reported the participants with unilateral LE than the corresponding side of con-
results by subgroups dened by age and gender. trols (p<0.001; gure 3).

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Figure 2 Forest plot for pressure pain thresholds.

Reaction time to lift the hand off a button task was 37.8 ms anthropometry/anatomy. This section presents differences
(95% CI 24.8 to 50.7, I2=54%) slower and two choice reaction between the contralateral limb of patients and data for control
time in a movement to a target task was 36.0 ms (95% CI 25.8 to participants (SMD and 95% CI of all included studies, web
46.1, I2=0%) slower in the contralateral side of patients than the only supplementary le B). All included studies of sensory,
corresponding side of controls (p<0.001; gure 4). Speed of move- motor and nociceptive systems and the majority of the muscle
ment was 20 cm/s (95% CI 35.3 to 4.6, I2=52%) slower in the strength studies investigated unilateral LE.
contralateral side of patients than controls (p<0.001; gure 4).
Motor measures
Appraisal A study of corticomotor excitability (resting motor threshold,
Studies unable to be included in the meta-analysis are consid- stimulus response curve, silent period and motor evoked poten-
ered in four key themes related to changes in (1) motor, tial), as measured by transcranial magnetic stimulation, demon-
(2) sensory and (3) nociceptive systems, as well as (4) variants in strated no differences between the affected or contralateral limb in

Figure 3 Forest plot for temperature pain thresholds.

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Figure 4 Forest plot for reaction time and speed of movement.

14 patients and 16 controls.26 Electromechanical delay during (mean 234 N86).23 All studies, except one31 demonstrated a sig-
gripping (n=13 patients and controls)27 is longer in patients nicant difference between sides within the patient group.23 27 29 30
contralateral side (mean: 6424 ms) compared with controls Studies of other strength measures have focused on upper
(mean: 3914 ms; p<0.001), while rate of force development (in limb tendinopathy, particularly unilateral LE. Isometric elbow
the same study) did not differ between the two groups. Evaluation exion and extension strength has been shown to be no differ-
of wrist position during a spontaneous gripping task in 40 patients ent between 164 patients with unilateral LE and 54 controls32
and 40 controls showed patients gripped in 11 (95% CI 7 to 14, (patientsexion; 246.740.4 N, extension 185.931.8 N;
p<0.001) more exion than controls, bilaterally.23 Two studies controlsexion; 245.740.4 N, extension; 185.932.3 N;
assessed one-choice reaction time of pointing to a target and SMD Flexion 0.02, SMD Extension 0.00). Wrist extension
speed-of-movement in patients compared to controls,25 28 which strength has been shown to be 24% less in 20 patients (87.0
could not be meta-analysed due to signicant heterogeneity, 40.3 N) than controls (114.030.3 N; SMD 0.75).30 Another
I=76% (p<0.001). Both demonstrated slower reaction time on study reported isometric strength measures of a range of upper
the contralateral side of the patients than the controls (13% (SMD limb muscles in 16 patients with unilateral LE and controls and
0.84) and 22% (SMD 1.13)).25 28 showed a strength decit of 1629% (table 1).31 There was no
Five studies investigated maximal grip strength, using a hand-held signicant difference between sides in the patients for any of the
dynamometer, in patients with unilateral LE,23 27 2931 which could strength measures ( p=>0.05).
not be meta-analysed due to signicant heterogeneity I=89% Isometric strength has also been assessed for unilateral rotator
(p<0.001). Three demonstrated a small (SMD 0.24 to cuff tendinopathy. Rather than a decrease, isometric shoulder
0.36),27 29 30 and one a large (SMD 2.38) reduction in strength in abduction strength was 15% greater in 10 patients with unilat-
patients than controls.31 The remaining study demonstrated a eral rotator cuff tendinopathy compared with 9 controls24
greater strength (SMD 0.59) in patients (28479N) than controls (patients: 22389 N; controls: 18963 N, SMD 0.44).

Table 1 Strength measures between the contralateral side of patient and healthy controls (meanSD)
Patient (n=16) Control (n=16) SMD 95% CI

Metacarpophalangeal joint extension 4116 N 5816 N 1.04 (0.29 to 1.78)


Metacarpophalangeal joint flexion 6736 N 9120 N 0.80 (0.08 to 1.53)
Wrist joint extension 7044 N 9724 N 0.74 (0.02 to 1.46)
Wrist joint flexion 9556 N 11924 N 0.54 (0.16 to 1.25)
Shoulder internal rotation 11364 N 14448 N 0.53 (0.17 to 1.24)
Shoulder external rotation 8140 N 9728 N 0.45 (0.25 to 1.15)
Shoulder abduction 12768 15140 N 0.42 (0.28 to 1.12)
SMD, standard mean difference, N, Newtons.

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Sensory measures speed of movement. These results align with ndings from
Proprioceptive acuity has been assessed by the ability to discrim- other studies that could not be included in the meta-analyses
inate between two weights between 100 and 130 g in steps of (due to study population or measurements) and studies of other
2 g increments using custom-built equipment.26 Webers frac- musculoskeletal conditions that demonstrate contralateral
tion, which expresses the acuity threshold (minimum difference sensory and motor system decits in patients with unilateral
in weight that can be detected) as a proportion of 100 g, was carpal tunnel syndrome,36 and chronic wrist pain.37 For
not different between the contralateral side of patients and con- instance, Fernandez-de-las-Penas36 reported lower pressure pain
trols (4.93.2%; and 5.42.1%, respectively, p>0.05),33 but thresholds over the peripheral nerves, the carpal tunnel and the
was less for the affected side (8.23.0%, p=0.001) than the C5C6 zygapophyseal joints of the non-affected side in women
contralateral side. with unilateral carpal tunnel syndrome than for pain-free con-
trols. Smeulders37 quantied motor control using a writing task
Nociceptive system measures with measures of uency, size and velocity of stroke patterns in
In contrast to the meta-analysis for pressure and temperature patients with unilateral chronic wrist pain and controls. The
pain thresholds, a study of electrical pain thresholds by means patients were signicantly less uent than the controls in both
of stimulation to the skin over extensor carpi radialis, in their affected and contralateral arm, suggesting bilateral motor
18 patients and 16 controls, demonstrated no signicant differ- system decits.
ence between the contralateral side of the patients and con- It is tempting to speculate that sensory system decits might
trols,34 but the affected side was signicantly more sensitive be attributed to abnormalities of central pain processing.
than the contralateral side. Central sensitisation arises from convergence of noxious and
Muscle trigger points have been assessed using a standardised non-noxious inputs on the wide dynamic range neurons in the
method by an experienced assessor blind to the patients condi- dorsal horn38 with subsequent enhanced sensitivity to painful
tion, in 25 patients and 20 controls.21 The number of latent (hyperalgesia) and normally non-painful (allodynia) stimuli over
trigger points in the contralateral side of patients (2.2, 95% CI an area extending beyond the injured segment. Central sensitisa-
1.8 to 2.6) was higher than that in controls (0.4, 95% CI 0.0 to tion is present in many chronic pain conditions such as bro-
0.07, p<0.001, SMD 0.89). myalgia, low back pain, complex regional pain syndrome,39
migraine, tension-type headache and myofascial pain syn-
drome.38 The widespread hyperalgesia extending to the contra-
Anatomic/anthropometric measures lateral limb in unilateral tendinopathy appears similar to that
In patients with patella tendinopathy,18 longitudinal arch height present in other chronic pain states.
of the foot, during maximum weight bearing is lower in patients Several mechanisms may explain the bilateral changes in
(42.07.4 mm) than controls (50.45.9 mm; SMD 1.29), but motor system function. First, it is well known that unilateral
there were no differences between sides within the patient exercise leads to strength and skill adaptations bilaterally
group (affected: 42.38.2 mm). There was no difference in an through a process known as cross education.40 Signicant
indirect measure of hamstring length or ankle dorsiexion gains in contralateral strength41 42 and skill43 have been shown
between groups. with unilateral exercise, regardless of whether it is active vol-
Two imaging studies used ultrasound to measure local itional, facilitated (electrical stimulation) or imagined. The
anatomy at the Achilles tendon (in unilateral mid-portion reverse, due to a unilateral reduction in activity might explain
Achilles tendinopathy)35 and the common extensor tendon of the effects in the contralateral side. The underlying mechanisms
the elbow (in LE),20 without blinding of the sonographer. The for cross education are poorly understood, but likely involve
thickness of the Achilles tendon was slightly greater and the spinal and supra-spinal centres. As H-reex amplitudes (which
echogenicity less on the contralateral side of 11 patients with largely depend on spinal motoneuron excitability) do not
Achilles tendinopathy (6.61.2 mm and 82.912.9 U, respect- change in the untrained muscle, despite strength gain4446
ively) than that of 9 controls (5.01.3 mm and 119.313.5 U, supra-spinal mechanisms are more likely. Relevant cortical
respectively; p=<0.05).35 The affected tendon (9.41.2 mm) mechanisms are thought to involve a complex network of inter-
was thicker than the contralateral tendon, but there was no dif- hemispheric connections and ipsilateral corticospinal bres from
ference in echogenicity (76.711.7 U). Another study investi- the primary motor cortex, which provide neural drive to the
gated the accuracy of power Doppler imaging for the diagnosis contralateral muscle during unilateral contraction.47 48
of unilateral LE.20 There was a tendency towards a thicker Corticospinal excitability (measured by transcranial magnetic
tendon on the contralateral side of patients (n=18) than con- stimulation) to hand muscles increase during contraction of the
trols (n=19), which was in the order of 0.50 mm (95% CI 0.00 opposite side,4951 which implies interhemispheric interactions.
to 0.99, p=0.05) or 11% of the control group mean tendon Functional MRI (fMRI) has demonstrated that changes in acti-
thickness (4.47 mm). This difference was comparable to the vation of the contralateral motor areas ( premotor and primary
15% greater thickness of the affected tendon (mean5.82 mm; motor cortex) are similar in both sides during unilateral activa-
difference0.86 mm (95% CI 1.35 to 0.36; p=0.002) than tion,5254 and unilateral exercise elicits activation in the contra-
the unaffected tendon in the LE group. lateral somatosensory54 and left temporal cortices (involved in
movement memory).52 This nding suggests that the somatosen-
DISCUSSION sory cortex may play a pivotal role in bilateral strength gains
This review provides a synthesis of research ndings of sensory with unilateral training. It remains unknown, but possible that
and motor differences, compared with pain-free controls, in the deconditioning of the affected limb in unilateral tendinopathy
limb contralateral to the side of symptoms in patients with uni- exhibits a negative form of cross education. This requires
lateral tendinopathy. In general, meta-analysis of data from mul- further investigation. Second, an alternative explanation for the
tiple studies provides evidence of signicant decits in the bilateral motor changes is that these features were different from
sensory and motor systems, including pressure and thermal pain the healthy controls in these individuals prior to the onset of
thresholds, simple reaction time, two-choice reaction time and tendinopathy and the motor differences could even contribute

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to the conditions development. This requires consideration in Contributors LH, PH and BV contributed to conception, design and construct of
longitudinal studies. the study. LH, EL and BV conducted the comprehensive search, critical appraisal and
analyses. All authors contributed to manuscript writing. BV and LH are guarantors of
The studies excluded from the meta-analysis demonstrated the overall content.
consistent lower grip strength on the contralateral side of
Funding Funding was provided by a Programme Grant (NHMRC Program Grant
patients with unilateral LE than controls in four of ve #631717) and Research Fellowship (PH) from the National Health and Medical
studies23 27 29 30 and medium-to-large strength decits at other Research Council of Australia and an Australian Postgraduate Award scholarship
distal and proximal joints of the upper limb.30 31 There were no (LH).
differences for the direct comparison of elbow exion and Competing interests None.
extension between the contralateral side of patients and the Provenance and peer review Not commissioned; externally peer reviewed.
controls.32
Two studies revealed a substantial increase in strength of the
contralateral side of patients compared with controls.23 24 One
REFERENCES
demonstrated increased grip strength on the contralateral side of 1 Selvanetti A, Cipolla M, Puddu G. Overuse tendon injuries: basic science and
patients with unilateral LE (SMD 0.59),23 whereas the other classication. Oper Tech Sports Med 1997;5:11017.
demonstrated increased shoulder abduction strength in patients 2 Skjong C, Meininger A, Ho S. Tendinopathy treatment: where is the evidence? Clin
with unilateral rotator cuff tendinosis (SMD 0.44).24 There Sports Med 2012;31:32950.
3 Cook JL, Khan KM, Purdam CR. Achilles tendinopathy. Man Ther 2002;7:12130.
are several possible explanations. First, it is possible that the 4 Astrm M, Rausing A. Chronic Achilles tendinopathy. A survey of surgical and
augmented strength is secondary to a compensatory increase in histopathologic ndings. Clin Orthop Relat Res 1995;316:15164.
the functional use of the unaffected side to protect the injured 5 Egerbacher M, Arnoczky SP, Caballero O, et al. Loss of homeostatic tension induces
limb. Second, the patient group might have been stronger than apoptosis in tendon cells: an in vitro study. Clin Orthop Relat Res
2008;466:15628.
the controls prior to the development of the unilateral tendino-
6 Alfredson H, Harstad H, Haugen S, et al. Sclerosing polidocanol injections to treat
pathy as a result of activity, which may underpin the increased chronic painful shoulder impingement syndrome-results of a two-centre collaborative
use of the limb leading to the tendinopathy.23 Both scenarios pilot study. Knee Surg Sports Traumatol Arthrosc 2006;14:13216.
could be addressed by the adoption of a prospective longitu- 7 Knobloch K. The role of tendon microcirculation in Achilles and patellar
dinal study design. tendinopathy. J Orthop Surg 2008;3:1830.
8 Backman C, Boquist L, Fridn J, et al. Chronic Achilles paratenonitis with
Bilateral sensory and motor system decits in unilateral tendi- tendinosis: an experimental model in the rabbit. J Orthop Res 1990;8:5417.
nopathy require consideration in both clinical practice and 9 Soslowsky LJ, Thomopoulos S, Tun S, et al. Overuse activity injures the
research for several reasons. First, the ndings of this review supraspinatus tendon in an animal model: a histologic and biomedical study. J
highlight the importance of inclusion of a healthy matched Shoulder Elbow Surg 2000;9:7984.
10 Barbe MF, Barr AE, Gorzelany I, et al. Chronic repetitive reaching and grasping
control group for comparison in studies of features of tendino-
results in decreased motor performance and widespread tissue responses in a rat
pathy. Second, the presence of differences relative to controls on model of MSD. J Orthop Res 2003;21:16776.
both the symptomatic and non-symptomatic sides suggests that 11 Andersson G, Forsgren S, Scott A, et al. Tenocyte hypercellularity and vascular
there could be benet from rehabilitation that addresses motor proliferation in a rabbit model of tendinopathy: Contralateral effects suggest the
and sensory system features on both sides. Specic training of involvement of central neuronal mechanisms. Br J Sports Med 2011;45:399406.
12 Genaidy AM, LeMasters GK, Lockey J, et al. An epidemiological appraisal
the contralateral limb may also provide additional benets to instrumenta tool for evaluation of epidemiological studies. Ergonomics
the affected limb through cross education, through the mechan- 2007;50:92060.
ism discussed above. Third, patients participating in sports or 13 Landis JR, GG Kock. The measurement of observer agreement for categorical data.
occupations requiring rapid bilateral reaction time and move- Biometrics 1977;33:15974.
14 Cohen J. Statistical power analysis for the behavioral sciences. 2nd edn. Hillsdale,
ment speed such as trap shooting and boxing, may require spe-
NJ: Erlbaum, 1988.
cically targeted training to address decits that may present 15 Chourasia AO, Buhr KA, Rabago DP, et al. The effect of lateral epicondylosis on
bilaterally. upper limb mechanical parameters. Clin Biomech (Bristol, Avon) 2012b;27:12430.
This review has some limitations, which require consider- 16 Alizadehkhaiyat O, Fisher A, Kemp G, et al. Assessment of functional recovery in
ation. The meta-analyses included only a small number of tennis elbow. J Electromyogr Kinesiol 2009;19:6318.
17 Strizak AM, Gleim GW, Sapega A, et al. Hand and forearm strength and its relation
studies with small sample sizes and of only one tendinopathy to tennis. Am J Sports Med 1983;11:2349.
(ie, LE). There is a clear need for additional studies with larger 18 Crossley KM, Thancanamootoo K, Metcalf BR, et al. Clinical features of patellar
sample sizes across a range of tendinopathies. The quality of tendinopathy and their implications for rehabilitation. J Orthop Res
studies varied substantially and was overall quite low. A key limi- 2007;25:116475.
19 Dauty M, Dupr M, Potiron-Josse M, et al. Identication of mechanical
tation was the lack of conrmation of localised tendinopathy
consequences of jumpers knee by isokinetic concentric torque measurement in elite
using diagnostic imaging. Only two studies required conrm- basketball players. Isokinetics Exerc Sci 2007;15:3741.
ation of pathology with diagnostic imaging for inclusion into 20 Du Toit C, Stieler M, Saunders R, et al. Diagnostic accuracy of power Doppler
the study, and even then neither reported the measures reliabil- ultrasound in patients with chronic tennis elbow. Br J Sports Med 2008;42:8726.
ity and only one used diagnostic imaging to verify healthy 21 Fernndez-Carnero J, Fernndez-De-Las-Peas C, La Llave-Rincn AI, et al. Bilateral
myofascial trigger points in the forearm muscles in patients with chronic unilateral
tendon in controls. lateral epicondylalgia: a blinded, controlled study. Clin J Pain 2008;24:8027.
In conclusion this review highlights that sensory and motor 22 Gaida JE, Cook JL, Bass SL, et al. Are unilateral and bilateral patellar tendinopathy
system decits are common in the non-injured limb of patients distinguished by differences in anthropometry, body composition, or muscle strength
with unilateral tendinopathy, particularly in LE, which has in elite female basketball palyers? Br J Sports Med 2004;38:5815.
23 Bisset LM, Russell T, Bradley S, et al. Bilateral sensorimotor abnormalities in
received most attention in literature. These data suggest involve-
unilateral lateral epicondylalgia. Arch Phys Med Rehabil 2006;87:4905.
ment of the central nervous system in sensory and motor decits 24 Brox JI, Re C, Saugen E, et al. Isometric adbuction muscle activation in patients
seen in unilateral tendinopathy, which likely contribute to the with rotator tendinosis of the shoulder. Arch Phys Med Rehabil 1997;87:12607.
expression of pain and disability. The results clearly demonstrate 25 Bisset LM, Coppieters MW, Vicenzino B. Sensorimotor decits remain despite
that the contralateral side of the body cannot be used as a refer- resolution of symptoms using conservative treatment in patients with tennis elbow:
a randomized controlled trial. Arch Phys Med Rehabil 2009;90:18.
ence standard for assessment, either in clinical practice or 26 Dessureault L, Tremblay F, Bilodeau M. Chapter one: corticomotor excitability and
research and that treatments other than those that target local manual dexterity in chronic lateral epicondylalgia, in School of Human Kinetics.
pathology are likely to be required. University of Ottawa, 2008.

Heales LJ, et al. Br J Sports Med 2013;0:18. doi:10.1136/bjsports-2013-092535 7


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Review

27 Chourasia AO, et al. Effect of lateral epicondylosis on grip force development. 45 Lagerquist O, Zehr EP, Docherty D. Increased spinal reex excitability is not
J Hand Ther 2012;25:2737. associated with neural plasticity underlying the cross-education effect. J Appl Physiol
28 Pienimki TT, Kauranen K, Vanharanta H. Bilaterally decreased motor performance 2006;100:8390.
of arms in patients with chronic tennis elbow. Arch Phys Med Rehabil 46 Fimland MS, Helgerud J, Solstad GM, et al. Neural adaptations underlying
1997;78:10925. cross-education after unilateral strength training. Eur J Appl Physiol
29 Coombes B, Bisset L, Vicenzino B. Thermal hyperalgesia distinguishes those with severe 2009;107:72330.
pain and disability in unilateral lateral epicondylalgia. Clin J Pain 2012;28:595601. 47 Carroll TJ, Herbert RD, Munn J, et al. Contralateral effects of unilateral
30 Slater H, et al. Sensory and motor effects of experimental muscle pain in patients strength training: evidence and possible mechanisms. J Appl Physiol 2006;101:
with lateral epicondylalgia and controls with delayed onset muscle soreness. Pain 151422.
2005;114:11830. 48 Carson RG. Neural pathways mediating bilateral interactions between the upper
31 Alizadehkhaiyat O, et al. Upper limb muscle imbalance in tennis elbow: a functional limbs. Brain Res Rev 2005;49:64162.
and electromyographic assessment. J Orthop Res 2007;25:16517. 49 Muellbacher W, Facchini S, Boroojerdi B, et al. Changes in motor cortex excitability
32 Coombes B, Bisset L, Vicenzino B. Elbow exor and extensor muscle weakness in during ipsilateral hand muscle activation in humans. Clin Neurophysiol
lateral epicondylalgia. Br J Sports Med 2012;46:44953. 2000;111:3449.
33 Dessureault L, Tremblay F, Bilodeau M. Chapter two: weight discrimination in chronic 50 Stedman A, Davey NJ, Ellaway PH. Facilitation of human rst dorsal interosseous
lateral epicondylalgia, in School of Human Kinetics. University of Ottawa, 2008. muscle responses to transcranial magnetic stimulation during voluntary contraction
34 Lundeberg T, Abrahamsson P, Bondesson L, et al. Effect of vibratory stimulation on of the contralateral homonymous muscle. Muscle Nerve 1998;21:10339.
experimental and clinical pain. Scand J Rehabil Med 1988;20:14959. 51 Stinear CM, Walker KS, Byblow WD. Symmetric facilitation between motor
35 Grigg NL, Wearing SC, Smeathers JE. Achilles tendinopathy has an aberrant strain cortices during contraction of ipsilateral hand muscles. Exp Brain Res
response to eccentric exercise. Med Sci Sports Exerc 2012;44:1217. 2001;139:1015.
36 Fernndez-de-las-Peas C, de la Llave-Rincn AI, Fernndez-Carnero J, et al. 52 Farthing JP, Borowsky R, Chilibeck PD, et al. Neuro-physiological adaptations
Bilateral widespread mechanical pain sensitivity in carpal tunnel syndrome: evidence associated with cross-education of strength. Brain Topogr 2007;20:7788.
of central processing in unilateral neuropathy. Brain 2009;132:14729. 53 Kristeva R, Cheyne D, Deecke L. Neuromagnetic elds accompanying unilateral and
37 Smeulders MJC, Kreulen M, Hage JJ, et al. Motor control impairment of the bilateral voluntary movements: Topography and analysis of cortical sources.
contralateral wrist in patients with unilateral chronic wrist pain. Am J Phys Med Rehabil Electroencephalogr Clin Neurophysiol 1991;81:28498.
2002;81:17781. 54 Huang L, Zhou S, Li X, et al. A functional MRI investigation of bilateral cortical
38 Yunus MB. Fibromyalgia and overlapping disorders: the unifying concept of central activation during unilateral voluntary motor activity and electromyostimulation. J Sci
sensitivity syndromes. Semin Arthritis Rheum 2007;36:33956. Med Sport 2006;9(Supplement):15.
39 Henry DE, Chiodo AE, Yang W. Central nervous system reorganization in a variety of 55 Fernndez-Carnero J, Fernndez-de-las-Peas C, Sterling M, et al. Exploration of the
chronic pain states: a review. Phys Med Rehabil 2011;3:111625. extent of somato-sensory impairment in patients with unilateral lateral
40 Lee M, Carroll TJ. Cross education: possible mechanisms for the contralateral effects epicondylalgia. J Pain 2009;10:117985.
of unilateral resistance training. Sports Med 2007;37:114. 56 Fernndez-Carnero J, Fernndez-De-Las-Peas C, de la Llave-Rincn AI, et al.
41 Zhou S. Chronic neural adaption to unilateral exercise: mechanisms of cross Widespread mechanical pain hypersensitivity as sign of central sensitization in
education. Exerc Sports Sci Rev 2000;28:17784. unilateral epicondylalgia a blinded, controlled study. Clin J Pain 2009;25:55561.
42 Hortobgyi T, Lambert NJ, Hill JP. Greater cross education following training with 57 Fernndez-de-las-Peas C, Ortega-Santiago R, Ambite-Quesada S, et al. Specic
muscle lengthening than shortening. Med Sci Sports Exerc 1997;29:10712. mechanical pain hypersensitivity over peripheral nerve trunks in women with
43 Kim K, Cha YJ, Fell DW. The effect of contralateral training: inuence of unilateral unilateral epicondylalgia and carpal tunnel syndrome. J Orthop Sports Phys Ther
isokinetic exercise on one-legged standing balance of the contralateral lower 2010(Journal Article).
extremity in adults. Gait Posture 2011;34:1036. 58 Ruiz-Ruiz B, Fernndez-de-Las-Peas C, Ortega-Santiago R, et al. Topographical
44 Dragert K, Zehr EP. Bilateral neuromuscular plasticity from unilateral training of the pressure and thermal pain sensitivity mapping in patients with unilateral lateral
ankle dorsiexors. Exp Brain Res 2011;208:21727. epicondylalgia. J Pain 2011;12:10408.

8 Heales LJ, et al. Br J Sports Med 2013;0:18. doi:10.1136/bjsports-2013-092535


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Sensory and motor deficits exist on the


non-injured side of patients with unilateral
tendon pain and disabilityimplications for
central nervous system involvement: a
systematic review with meta-analysis
L J Heales, E C W Lim, P W Hodges, et al.

Br J Sports Med published online October 21, 2013


doi: 10.1136/bjsports-2013-092535

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