Sports Med (2016) 46:18331845
DOI 10.1007/s40279-016-0539-4
SYSTEMATIC REVIEW
Forearm Muscle Activity in Lateral Epicondylalgia: A Systematic
Review with Quantitative Analysis
Luke J. Heales1,2 Michael J. G. Bergin1
Bill Vicenzino1 Paul W. Hodges1
Published online: 22 April 2016
Springer International Publishing Switzerland 2016
Abstract
Background Lateral epicondylalgia (LE) refers to pain at
the lateral elbow and is associated with sensory and motor
impairments that may impact on neuromuscular control
and coordination.
Objective This review aimed to systematically identify
and analyse the literature related to the comparison of
neuromuscular control of forearm muscles between indi-
viduals with and without LE.
Methods A comprehensive search of electronic databases
and reference lists using keywords relating to neuromus-
cular control and LE was undertaken. Studies that inves-
tigated electromyography (EMG) measures of forearm
muscles in individuals with symptoms of LE were included
if the study involved comparison with pain-free controls.
The Epidemiological Appraisal Instrument was used to
assess study quality. Data extracted from each study were
used to calculate the standardised mean difference and
95 % confidence intervals to investigate differences
between groups.
Electronic supplementary material The online version of this
article (doi:10.1007/s40279-016-0539-4) contains supplementary
material, which is available to authorized users.
& Paul W. Hodges
p.hodges@uq.edu.au
1
NHMRC Centre of Clinical Research Excellence in Spinal
Pain, Injury and Health, School of Health and Rehabilitation
Science, The University of Queensland, Brisbane, QLD 4072,
Australia
2
School of Human, Health and Social Sciences, Division of
Physiotherapy, Central Queensland University,
Rockhampton, QLD 4701, Australia
Results The search revealed a total of 1920 studies, of
which seven were included from 44 that underwent
detailed review. Due to differences in outcome measures
and tasks assessed, meta-analysis was not possible. The
seven included studies used 60 different EMG outcomes, of
which 16 (27 %) revealed significant differences between
groups. Two were properties of motor unit potentials dur-
ing wrist extension. Four were measures of increased time
between recruitment of wrist extensor muscles and onset of
grip force. Seven were measures of amplitude of EMG
during tennis strokes. Three were measures of motor cortex
organisation.
Conclusion Features of neuromuscular control differ
between individuals with LE and pain-free controls. This
implies potential central nervous system involvement and
indicates that rehabilitation may be enhanced by consid-
eration of neuromuscular control in addition to other
treatments.
Key Points
Some features of neuromuscular control appear
different between individuals with and without
lateral epicondylalgia and these could imply central
nervous system involvement in the condition.
Systematic review of the literature revealed evidence
of differences in 16 of 60 unique electromyography
measures in seven studies.
Widely disparate measurement methods precluded
meta-analysis of data, but reveal differences across a
range of tasks.
123
1834 L. J. Heales et al.

1 Introduction 2.2 Study Selection

Upon retrieval from the above search strategy, all titles and
Lateral epicondylalgia (LE), or tennis elbow, refers to pain
abstracts were screened to identify studies that included
at the lateral epicondyle and is characterised by pain and
EMG outcomes in individuals with LE and comparison
decreased strength during gripping [1, 2]. This condition
with pain-free controls. It was decided a priori that any
impacts on participation in recreational and occupational
measures of forearm muscle EMG in individuals with LE
activities [3, 4]. Although commonly unilateral in presen-
should be included provided there was comparison with a
tation, LE is associated with bilateral changes of some
pain-free control group. The full text was obtained for all
elements of the motor system. Examples include gripping
eligible studies. A detailed evaluation using pre-determined
with the wrist in a less extended position than pain-free
criteria based on study design, diagnosis of LE and reports
controls [5], deficits in upper limb strength [6], altered fine
of EMG outcome measures was undertaken. Reviews, case
motor control (measured by the Purdue Pegboard Test and
studies, and letters to the editor were excluded. Clarifica-
Complete Manual Dexterity Test) [7], slower reaction time
tions on matters of eligibility were made by discussion with
[5, 8], and slower speed of movement [5, 8]. This diverse
another investigator.
array of differences in the motor system between individ-
uals with and without LE is likely to be related to modified
2.3 Quality Assessment
neuromuscular control of forearm muscles.
Neuromuscular control is often quantified using record-
Two assessors (LH, MB) used the modified Epidemiolog-
ings of myoelectric activity [9, 10] as a measure of the net
ical Appraisal Instrument (EAI) to independently score the
output of the processes in the central nervous system (CNS).
quality of the included studies [11]. The EAI is valid and
Investigation of neuromuscular control associated with LE is
reliable for appraisal of observational studies [11]. The
likely to aid development of an understanding of potential
design of the included studies precluded relevance of items
impairments in the motor system and inform the develop-
related to randomisation, follow-up and environmental
ment of targeted treatments. There is evidence that neuro-
variables and these items were excluded from the assess-
muscular control in individuals with LE differs from that of
ment and the EAI was condensed to 33 items of a possible
pain-free controls, but methods and findings are diverse. The
43 items. Prior to the quality evaluation, detailed criteria to
primary aim of this study was to systematically review the
determine each response were modified from the original
literature regarding changes in myoelectric activity of the
tool to match the purpose of this review and agreed upon
forearm muscles in LE. Human studies of electromyography
by all investigators. A third party (BV) was consulted for
(EMG) recordings of forearm muscles in individuals with LE
disagreements between the two assessors. Each item was
(bilateral and unilateral) that included a comparison with
independently scored using the standardised scale: yes
pain-free controls were included in this review.
(score = 1), partial (score = 0.5), no (score = 0), unable
to determine (score = 0), or not applicable (item was
removed from scoring) and the average used as the indi-
2 Methods
cator of the overall quality assessment score for each study
(range 01).
2.1 Search Strategy
2.4 Data Extraction
Electronic databases (Medlinevia Ovid, PubMed and
Scopus) were searched to identify all English-language
LH undertook data extraction, and any queries were dis-
studies for all years up to July 2015. Keyword, title and
cussed and resolved by all investigators. Data pertaining to
abstract information were used. Search terms were the
the sample population and study methodology as well as
condition of interest (e.g. tennis elbow, epicondyl*) and
the descriptive data of the reported EMG outcome mea-
common terms used to describe neuromuscular control (e.
sures were extracted. All EMG measures that compared
g. electromy*, EMG, motor control) (wildcard * repre-
participants with LE (symptomatic or asymptomatic limb)
sents any letters). The reference lists of all included studies
and pain-free individuals were included. All EMG mea-
were systematically hand-searched to identify articles that
sures were considered relevant (e.g. root mean squared
may have been missed by the initial screening. This pro-
[RMS] amplitude, median frequency). Authors were con-
cess included articles not on electronic databases, articles
tacted if additional information was required.
from networks or conferences, and theses and books.

123
 Table 1 Characteristics of included studies
Study Participants DOS Affected Task Outcome measures Muscle recorded Electrodes
(number) (weeks) arm

Alizadehkhaiyat Controls (16) NR D = 16 Sustained isometric grip at 50 % Root mean squared amplitude ECR, EDC, FCU, FDS Surface
et al. [6] LE (16) ND = 0 MVC Median frequency
Bauer and Murray Controls (6) NR NR Single-handed backhand tennis Mean activation times ECRB, FCU, TB Surface
Forearm Muscle Activity in Lateral Epicondylalgia

[15] LE (10) volley

Calder et al. [17] Controls (37) 169 (130) NR Resisted wrist extension at 510 % Needle- and surface-detected motor ECRB Surface and
LE (11) MVC unit potentials intramuscular
Chourasia et al. Controls (13) 104 (26 Unilateral Maximum isometric grip as rapidly Temporal parameters ECR Surface
[20] Unilateral LE 521) D = 11 as possible
(11) ND = 2
Bilateral LE
(15)
Dessureault et al. Controls (16) 63 (69) D = 10 Relaxation Corticomotor excitability ECR Surface
[16] LE (14) ND = 4
Kelley et al. [19] Controls (14) NR NR Single-handed backhand tennis Root mean squared amplitude ECRB, ECRL, EDC, Intramuscular
LE (16) stroke FCR, PT
Schabrun et al. [18] Controls (11) 38.3 D=7 Relaxation Corticomotor excitability ECRB, EDC Surface
LE (11) (29.4) ND = 4
D dominant, DOS duration of symptoms, ECR extensor carpi radialis, ECRB extensor carpi radialis brevis, ECRL extensor carpi radialis longus, EDC extensor digitorum communis, FCR flexor
carpi radialis, FCU flexor carpi ulnaris, FDS flexor digitorum superficialis, LE lateral epicondylalgia, MVC maximum voluntary contraction, ND non-dominant, NR not reported, PT pronator
teres, TB triceps brachii
1835

123
1836
Fig. 1 Flow chart for inclusion into the review. EMG electromyographic
2.5 Statistical Methods
The reliability of the quality assessment was evaluated
using SPSS V21 software (SPSS Inc, Chicago, IL, USA).
Kappa statistics were used to report the inter-rater relia-
bility between the two assessors. Inter-rater reliability was
considered as poor (\0.00), slight (0.000.2), fair (0.21
0.4), moderate (0.410.6), substantial (0.610.8), or almost
perfect (0.811.0) [12]. Meta-analysis was not possible due
to heterogeneity between studies with respect to the tasks
and outcome measures included in the studies (Table 1). To
123
L. J. Heales et al.
enable consistent comparison between findings of indi-
vidual studies and outcome measures, the standardised
mean difference (SMD) and 95 % confidence interval (CI)
were calculated and interpreted as small (0.2), medium
(0.5) and large (0.8) effect size [13]. If the 95 % CI did not
include zero, the outcome was considered statistically
significant. A positive SMD reflects greater values in LE
group than controls and vice versa. Because of the small
sample sizes of the included studies, we also calculated
90 % CIs. If the 90 % CI did not contain zero the outcome
was considered to be nearly significant.
Forearm Muscle Activity in Lateral Epicondylalgia
3 Results
3.1 Database Search
The comprehensive search strategy yielded a total of 1920
publications from electronic databases and hand-searched
reference lists (Fig. 1). All titles and abstracts were
screened and 44 potentially relevant studies were identi-
fied. Of these, eight satisfied the inclusion criteria and
reported EMG outcomes in participants with LE and
included comparison with a pain-free control group. One
study was excluded as it reported EMG of the hamstring
muscles during the nociceptive flexion reflex in partici-
pants with LE and no recordings from the forearm muscles
[14]. Exclusion of this study left seven studies that satisfied
the criteria for inclusion in this review. Two authors were
contacted to provide additional information as data were
only presented graphically. One study [15] was unable to
provide data due to technological advances since publica-
tion (i.e. the inability to retrieve data from floppy disc
storage media). The other study [16] provided the mean
and standard deviation for the outcomes of interest and
permission to publish these data.
3.2 Study Characteristics
Study characteristics are shown in Table 1. The location of
the study, year of publication, sample size and methodology
varied widely. Three studies (43 %) were conducted in the
United States, two in Canada (28 %), and one each in the
United Kingdom (14 %) and Australia (14 %). Two studies
(28 %) were published prior to 2000; three (43 %) in the
2000s; and two (28 %) since 2010. Sample sizes varied from
16 [15] to 48 [17] participants. Overall, the number of LE
participants (total n = 104) was greater than the number of
controls (total n = 99). The mean duration of symptoms for
individuals with LE ranged from 38 [18] to 169 [17] weeks.
All studies used a case-control study design. The muscles
assessed using EMG differed between studies. All studies
described data as representative of both extensor carpi
radialis (ECR) brevis and longus combined, or selective for
extensor carpi radialis brevis (ECRB) alone. Three studies
[6, 18, 19] recorded EMG from extensor digitorum com-
munis (EDC), two [6, 15] from flexor carpi ulnaris (FCU)
and one each from flexor carpi radialis (FCR) [19], flexor
digitorum superficialis (FDS) [6], pronator teres (PT) [19]
and triceps brachii (TB) [15]. Only one study described
EMG recording from extensor carpi radialis longus (ECRL)
separately from ECRB [19]. Five studies used surface
electrodes alone [6, 15, 16, 18, 20], one study used intra-
muscular electrodes alone [19], and one study used both
surface and intramuscular electrodes [17] (Table 1).
1837
3.3 Quality Assessment
Agreement between the two reviewers was almost perfect
( = 0.90, p \ 0.001) [12] with 222 agreements out of 238
decisions. The quality assessment scores are presented in
Table S1 (see electronic supplementary material). The
quality assessment revealed only two studies [17, 20] (28 %)
that clearly described the study design with details assessed
using the EAI tool. No longitudinal or prospective studies
were identified. Only three studies [16, 17, 20] (43 %) clearly
described their study sample, including how and where they
recruited participants. One study [20] (14 %) reported an a
priori sample size calculation, and only one study [20] (14 %)
used diagnostic imaging as part of the eligibility criteria.
Three studies [15, 17, 19] (43 %) did not report duration of
symptoms and three studies [6, 15, 19] (43 %) did not report
data from validated pain and disability questionnaires (e.g.
Patient-Rated Tennis Elbow Evaluation Form). No studies
blinded the assessors to the condition of the participant. The
reviewers were unable to detect the timeframe over which
the participants were recruited for any of the seven studies.
Two studies [16, 18] (28 %) matched for age and sex to
facilitate comparability between groups (LE and controls).
Three studies [6, 15, 20] (43 %) displayed the age and sex of
the participants but did not use statistical tests to compare
groups. One study [17] (14 %) showed that the age of their
control group was significantly younger than their LE group.
One study [19] (14 %) used control participants from a
previous paper and did not mention their age, sex or arm
dominance. The reviewers were unable to establish the
validity or reliability of LE diagnosis in any study. Despite
the importance of using validated measures, no studies
reported the validity or reliability of their main outcome
measures. Only one study [20] (14 %) adjusted for individual
covariates (e.g. age, sex), and no studies reported the results
relative to severity of the condition.
3.4 Neuromuscular Control
No outcomes were investigated by more than one study
(Table S2, electronic supplementary material). Quantitative
analysis of the seven included studies revealed a total of 60
neuromuscular control outcomes, of which 16 (28 %) were
significant using the SMD and 95 % CI. The following sec-
tions present findings according to the four identified tasks/
measures: (1) resisted wrist extension, (2) gripping, (3) tennis
strokes and (4) transcranial magnetic stimulation (TMS).
3.4.1 Resisted Wrist Extension
One study investigated morphology of motor unit action
potentials of ECRB during resisted wrist extension (Table 2)
[17]. Although this study revealed a greater duration and
123
1838 L. J. Heales et al.

Table 2 Outcome measures and calculated SMD and 95 % CI for resisted wrist extension [17]
Outcome Muscle LE group Control group SMD 95 % CI
Mean SD N Mean SD N

NMUP amplitude (mV) ECRB 519 426.6 11 419 300.7 37 0.08 0.56 to 0.76
NMUP area-to-amplitude ratio ECRB 1.62 0.59 11 1.27 0.43 37 0.73 0.04 to 1.42a
NMUP duration (ms) ECRB 9.7 3.16 11 7.64 2.85 37 0.69 0.01 to 1.38a
NMUP firing rate (Hz) ECRB 13.86 2.71 11 14.98 2.97 37 0.38 1.06 to 0.30
NMUP number of phases ECRB 2.63 0.81 11 2.55 0.71 37 0.11 0.57 to 0.78
SMUP amplitude (mV) ECRB 111.14 109.53 11 113.73 90.73 37 0.03 0.70 to 0.65
SMUP area (mm) ECRB 502.7 518.7 11 593.9 507.4 37 0.18 0.85 to 0.50
SMUP duration (ms) ECRB 19.21 5.93 11 19.76 5.52 37 0.10 0.77 to 0.58
CI confidence interval, ECRB extensor carpi radialis brevis, LE lateral epicondylalgia, N number of participants, NMUP needle-detected motor
unit potential, SD standard deviation, SMD standardised mean difference, SMUP surface-detected motor unit potential
a
Significant difference between LE and controls

Table 3 Outcome measures and calculated SMD and 95 % CI for grip

Study Outcome Muscle LE group Control group SMD 95 % CI
Mean SD N Mean SD N

Alizadehkhaiyat et al. [6] RMS amplitude ECR 0 28 16 13 20 16 0.52 1.23 to 0.19

RMS amplitude EDC 11 36 16 13 32 16 0.06 0.75 to 0.64
RMS amplitude FCU 37 32 16 32 24 16 0.17 0.52 to 0.87
RMS amplitude FDS 32 24 16 27 16 16 0.24 0.46 to 0.93
Median frequency ECR 16 8 16 16 8 16 0.00 0.69 to 0.69
Median frequency EDC 15 8 16 15 8 16 0.00 0.69 to 0.69
Median frequency FCU 14 4 16 15 8 16 0.15 0.54 to 0.85
Median frequency FDS 12 4 16 15 12 16 0.33 0.52 to 0.19
Chourasia et al. [20] Delaybilateral dominant ECR 0.061 0.02 15 0.039 0.008 11 1.32 0.45 to 2.19a
Delaybilateral non-dominant ECR 0.065 0.033 15 0.039 0.014 11 0.94 0.11 to 1.77a
Delayunilateral symptomatic ECR 0.061 0.029 11 0.039 0.008 11 0.99 0.10 to 1.98a
Delayunilateral asymptomatic ECR 0.064 0.024 11 0.039 0.014 11 1.22 0.30 to 2.15a
CI confidence interval, ECR extensor carpi radialis (brevis and longus combined), EDC extensor digitorum communis, FCU flexor carpi ulnaris,
FDS flexor digitorum superficialis, LE lateral epicondylalgia, N number of participants, RMS root mean squared, SD standard deviation, SMD
standardised mean difference
a
Significant difference between LE and controls

greater area-to-amplitude ratio of motor unit action potentials
in the LE group than in pain-free controls [17], methodolog-
ical issues limit the ability to draw robust conclusions. First,
properties of motor unit action potential shape are affected by
proximity of the electrode to the muscle fibres and this was
impossible to control. Second, the LE participants were sig-
nificantly older (mean age 46.6 10.7 years) than the healthy
controls (27.1 5 years). This is problematic for comparison
as motor unit morphology changes with age, usually around
the fifth decade of life [21]. Third, the force of contraction was
not standardised between groups/participants (range from 5 to
10 % maximum voluntary contraction (MVC). As motor unit
recruitment depends on force [22], participants who per-
formed contractions at higher levels of force may have sys-
tematically recruited larger motor units. No other significant
differences were observed for motor unit action potentials
recorded with needle (e.g. amplitude, firing rate, number of
phases) or surface electrodes (e.g. amplitude, area and dura-
tion) (Table 2) [17].
3.4.2 Gripping
Two studies investigated aspects of neuromuscular control
during gripping (Table 3) [6, 20]. One investigated the change
in RMS amplitude over time, normalised to the start value,
and median frequency of ECR, EDC, FDS and FCU during a
submaximal grip at 50 % [range from 5 to 10 % maximum
voluntary contraction (MVC)] until exhaustion [6]. RMS
amplitude was calculated at 5-second intervals and assessed by
linear regression. Using the criterion of SMD and 95 % CI,

123
Forearm Muscle Activity in Lateral Epicondylalgia
there were no significant between-group differences in
amplitude of muscle activity over time (Table 3). This differs
from the outcome of the statistical analysis reported in the
study by Alizadehkhaiyat et al. [6], but we argue that reference
to SMD and 95 % CI is more robust. A major consideration of
this study is the interpretation that there is less RMS amplitude
in the ECR muscle during gripping in the LE group than in the
pain-free controls [6]. EMG amplitude was normalised to that
at the start of the sustained contraction and assessed by linear
regression. This method does not allow comparison of muscle
amplitude between groups as this initial value used for nor-
malisation may differ for each group and provides a reference
that is difficult to interpret. If the participants in the LE group
commenced the contraction with greater activity (start value),
they might have less ability to increase the RMS amplitude
over time, thus affecting the slope of the EMG change and the
statistical comparison of activity over time between groups.
Additionally, this study did not record whether the included
participants did or did not experience pain during the gripping
task. Although inclusion of a task at 50 % MVC may have
resulted in pain provocation for some participants, the lack of
recorded information and our inability to find significance
between groups render this difficult to interpret.
Another study investigated the delay in time from the
onset of ECR EMG to the onset of grip force development,
measured using a specialised multi-axis dynamometer,
with the task performed in response to a visual stimulus
[20]. Participants with unilateral and bilateral LE demon-
strated a longer delay between these two events, bilaterally,
than pain-free controls (i.e. both symptomatic and asymp-
tomatic arm were affected) (Table 3) [20]. Although the
authors used the term electromechanical delay (EMD) to
describe this finding, this is not entirely accurate as EMD is
defined as the time interval between the initiation of EMG
from a muscle and the first detectable force output that the
muscle produces [23]. In this study, the onset of force was
identified from grip force, which is initiated by the finger
flexor muscles [FDS and flexor digitorum profundus
(FDP)], and does not reflect the onset of wrist extension
force. The wrist extensor muscles [ECRB, ECRL, EDC,
and extensor carpi ulnaris (ECU)] will co-activate with the
finger flexors to stabilise the wrist [24], but this measure
cannot be used as a surrogate of wrist extensor force.
Rather than simple interpretation as a delay in transduction
from EMG to force, increase in the latency between ECRB
EMG and grip force could reflect altered coordination
between finger flexor and wrist extensor muscles between
participant groups.
3.4.3 Tennis Strokes
Two studies investigated neuromuscular control during
single-handed backhand tennis strokes [15, 19]. Analysis
1839
using our a priori criterion could only be conducted on
one study [19], as data from the other study were not
available due to technological advances since publication
(i.e. the inability to retrieve data from floppy disc storage
media) [15]. Between-group differences were observed
for muscle amplitude (expressed as a percentage of MVC)
during a single-handed backhand tennis stroke, which was
divided into six phases: (1) preparation, (2) early and (3)
late acceleration, (4) ball impact, and (5) early and (6) late
follow through [19]. During the preparation phase, the LE
group demonstrated greater ECRL and FCR EMG than
pain-free controls (Table 4). During ball impact, the LE
group demonstrated a greater ECRB, ECRL and PT EMG
than pain-free controls. During early follow through, the
LE group demonstrated a greater ECRB and PT EMG
than pain-free controls [19]. There were no between-
group differences for the early acceleration or the late
follow-through phases using the criteria of SMD and 95 %
CI. Using a more lenient 90 % CI, several measures could
be considered nearly significant: ECRB EMG was
greater in LE during the early acceleration phase (SMD
0.90, 90 %CI 1.67 to 0.13) and FCR EMG was greater
during the late follow-through phase (SMD 0.92, 90 % CI
0.151.69) [19].
The study, which presented data that could not be used to
calculate SMD, investigated temporal parameters for ECRB,
FCU and TB during a single-handed backhand tennis volley
at three ball speeds (low 11.94 m/s, medium 17.13 m/s, and
high 22.95 m/s) and three racket head locations (central, long
axis, and torsional) [15]. LE participants had greater EMG
duration and greater integrated ECRB EMG for each ball
speed and each racket location (p [ 0.05) than pain-free
controls. When EMG times were pooled across ball speeds
and racket locations and presented as values pre- and post-
ball impact, the LE group demonstrated an earlier ECRB
EMG onset during the pre-impact period and a longer
duration of EMG (later EMG offset) into the post-impact
period than pain-free controls [15]. No differences were
observed for FCU and TB. No studies recorded pain levels
during tennis strokes, making it difficult to interpret whether
pain influenced the forearm muscle activity or timing in
individuals with LE. Although there was no mention of pain
in either study, participants with LE may have developed
specific patterns of motor activity with repeated exposure to
previously painful activities.
3.4.4 Transcranial Magnetic Stimulation
Two studies investigated corticomotor measures using
TMS in individuals with LE and pain-free controls [16,
18]. One study revealed that, compared with pain-free
controls, participants with LE had a smaller separation
between the cortical representations of ECRB and EDC
123
1840 L. J. Heales et al.

Table 4 Outcome measures and calculated SMD and 95 % CI for tennis strokes [19]
Outcome Muscle LE group Control group SMD 95 % CI
Mean SD N Mean SD N

RMS amplitudepreparation ECRB 28 23 8 18 11 14 0.59 0.31 to 1.48

RMS amplitudepreparation ECRL 28 19 8 13 10 14 1.04 0.11 to 1.98a
RMS amplitudepreparation EDC 13 9 8 11 7 14 0.25 0.62 to 1.12
RMS amplitudepreparation FCR 27 26 8 9 5 14 1.09 0.15 to 2.03a
RMS amplitudepreparation PT 14 12 8 13 12 14 0.08 0.79 to 0.95
RMS amplitudeearly acceleration ECRB 28 12 8 62 44 14 0.90 1.82 to 0.01
RMS amplitudeearly acceleration ECRL 36 40 8 35 23 14 0.03 0.84 to 0.90
RMS amplitudeearly acceleration EDC 44 33 8 57 39 14 0.34 1.21 to 0.54
RMS amplitudeearly acceleration FCR 19 18 8 14 17 14 0.28 0.60 to 1.15
RMS amplitudeearly acceleration PT 11 17 8 16 17 14 0.28 1.16 to 0.59
RMS amplitudelate acceleration ECRB 78 31 8 83 37 14 0.14 1.01 to 0.73
RMS amplitudelate acceleration ECRL 81 47 8 72 38 14 0.21 0.66 to 1.08
RMS amplitudelate acceleration EDC 81 31 8 77 19 14 0.16 0.71 to 1.03
RMS amplitudelate acceleration FCR 53 47 8 38 27 14 0.41 0.47 to 1.29
RMS amplitudelate acceleration PT 17 15 8 29 22 14 0.58 1.47 to 0.31
RMS amplitudeball impact ECRB 94 42 8 40 31 14 2.02 0.93 to 3.11a
RMS amplitudeball impact ECRL 89 29 8 43 43 14 1.14 0.20 to 2.09a
RMS amplitudeball impact EDC 42 25 8 72 55 14 0.62 1.51 to 0.27
RMS amplitudeball impact FCR 70 52 8 56 34 14 0.33 0.55 to 1.20
RMS amplitudeball impact PT 60 26 8 26 25 14 1.29 0.32 to 2.26a
RMS amplitudeearly FT ECRB 67 27 8 43 19 14 1.04 0.11 to 1.98a
RMS amplitudeearly FT ECRL 62 25 8 42 27 14 0.73 0.17 to 1.63
RMS amplitudeearly FT EDC 45 18 8 50 27 14 0.20 1.07 to 0.67
RMS amplitudeearly FT FCR 53 28 8 41 24 14 0.45 0.43 to 1.33
RMS amplitudeearly FT PT 61 32 8 32 20 14 1.12 0.18 to 2.06a
RMS amplitudelate FT ECRB 28 24 8 18 13 14 0.55 0.34 to 1.43
RMS amplitudelate FT ECRL 23 14 8 15 12 14 0.60 0.29 to 1.50
RMS amplitudelate FT EDC 16 12 8 21 12 14 0.40 1.28 to 0.48
RMS amplitudelate FT FCR 23 19 8 11 7 14 0.92 0.00 to 1.84
RMS amplitudelate FT PT 24 26 8 13 9 14 0.62 0.27 to 1.51
CI confidence interval, ECRB extensor carpi radialis brevis, ECRL extensor carpi radialis longus, EDC extensor digitorum communis, FCR flexor
carpi radialis, FT follow through, LE lateral epicondylalgia, N number of participants, PT pronator teres, RMS root mean squared, SD standard
deviation, SMD standardised mean difference
a
Significant difference between LE and controls

and fewer peaks of excitability in the motor cortex maps 4 Discussion

for ECRB and EDC (Table 5) [18]. The other study found
no significant differences for any measures of cortico-
motor excitability (e.g. motor-evoked potential [MEP],
resting motor threshold and silent period) [16].
When the data were analysed using a 90 % CI,
several additional measures approached significance.
Compared with pain-free controls, individuals with LE
showed a greater motor cortex map volume for ECRB
(SMD 0.89, 90 % CI 0.141.63) and a greater peak
MEP amplitude for ECRB (SMD 0.88, 90 % CI 0.14
1.62) [18].
The primary aim of this review was to systematically analyse
evidence for differences in the activity of forearm muscles
between individuals with and without LE. Quantitative anal-
ysis of data from multiple studies showed 60 outcome mea-
sures, of which 16 (27 %) of these differ significantly between
individuals with LE and pain-free controls. Of these 16 out-
comes, two were properties of motor unit potentials during
resisted wrist extension; four were measures of increased time
between recruitment of wrist extensor muscles and onset of
grip force; seven were measures of amplitude of EMG during

123
Forearm Muscle Activity in Lateral Epicondylalgia 1841

Table 5 Outcome measures and calculated SMD and 95 % CI for corticomotor measures
Study Outcome Muscle LE group Control group SMD 95 % CI
Mean SD N Mean SD N

Dessureault et al. MEPs ECR 101.28 79.53 15 115.6 103.67 16 0.15 0.86 to 0.56
[16] Resting motor threshold ECR 39.4 8.76 15 40.5 7.65 16 0.13 0.84 to 0.57
Silent period ECR 75 29.84 15 72.56 19.15 16 0.10 0.61 to 0.80
Schabrun et al. [18] Distance between COG for ECRB/EDC 0.11 0.05 11 0.20 0.10 11 1.10 2.00 to 0.19a
ECRB and EDC
Cortical volume ECRB 15.5 13.1 11 6.4 4.9 11 0.89 0.00 to 1.77
Cortical volume EDC 9.3 5.5 11 8.2 5.6 11 0.19 0.65 to 1.03
Peak MEP amplitude ECRB 1.3 0.79 11 0.71 0.46 11 0.88 0.01 to 1.76
Peak MEP amplitude EDC 0.82 0.35 11 0.64 0.37 11 0.48 0.37 to 1.33
Number of cortical peaks ECRB 1.4 0.8 11 3.4 1.5 11 1.60 2.43 to 0.77a
Number of cortical peaks EDC 1.8 1.0 11 3.2 1.5 11 1.06 1.82 to 0.30a
CI confidence interval, COG centre of gravity, ECR extensor carpi radialis (brevis and longus combined), ECRB extensor carpi radialis brevis,
EDC extensor digitorum communis, LE lateral epicondylalgia, MEP motor-evoked potential, N number of participants, SD standard deviation,
SMD standardised mean difference
a
Significant difference between LE and controls

single-handed backhand tennis strokes; and three were mea-
sures of motor cortex organisation.
4.1 Interpretation of Differences in Forearm Muscle
Activity in Lateral Epicondylalgia
4.1.1 Gripping
A surprising observation of this review is the paucity of
studies that have investigated forearm muscle activity during
gripping, despite the fact that pain during gripping is a pri-
mary clinical complaint in individuals with LE. Several
impairments in kinematics and force have been identified in
individuals with LE during gripping (e.g. altered wrist
position during gripping [5], decreased grip strength [6, 20]),
but only two studies have investigated forearm muscle
activity [6, 20]. No studies have investigated for possible
differences in EMG amplitude during gripping. Although
Alizadehkhaiyat et al. [6] reported a smaller increase in RMS
amplitude over time in ECR (normalised to the amplitude at
the start of the sustained contraction) in individuals with LE
than in controls, this did not reach our a priori defined
threshold for significance based on SMD and 95 % CI.
Further, as mentioned earlier, normalisation to the amplitude
at the start of the contraction, and the statistical analysis
using linear regression to determine between-group differ-
ences, render the data difficult to interpret.
Differences in temporal parameters have been identified
with gripping, but there is some confusion regarding the
interpretation of the data. The latency between the onset of
ECR EMG and the onset of grip force during rapid gripping
is longer, bilaterally, in individuals with unilateral and
bilateral LE than in pain-free controls [20]. Although this
was interpreted as increased EMD, the onset of force was
not that generated by the homonymous muscle. Rather than
reflecting the change in transduction of EMG to force gen-
erated by the same muscle (which is the traditional definition
of EMD), increased delay between the onset of ECR EMG
and force generated by the finger flexor muscles might
instead indicate a change in inter-muscle coordination,
mediated by either; (1) earlier activation of the ECR muscle,
or (2) delayed activation of the finger flexor muscles.
Although reaction time of finger flexor muscles was not
directly assessed during that study, the rate of force devel-
opment was reduced in individuals with LE. This may be
argued to indicate a potential slower activation of finger
flexor muscles. This reduced rate of force development (and
possibly slower activation of finger flexor muscles) might be
explained by differences in the task between groups. The LE
group were instructed to grip as rapidly and as hard as
possible, but stop prior to the onset of pain (i.e. pain-free
grip), whereas pain-free participants were instructed to grip
to maximum. The objective to stop prior to the onset of pain
might prevent the individuals in the LE group from gripping
as rapidly and as hard as possible. This may be compounded
by fear of pain, which has been shown to limit maximum
contractions [25]. Although a reduced rate of force devel-
opment was reported (potentially supporting this interpre-
tation) [20], this is only observed in the symptomatic arm of
individuals with LE and cannot explain the bilateral changes
in activation. Another possible explanation is the observa-
tion that individuals with LE actively grip with less wrist

123
1842
extension (i.e. closer to the neutral position), bilaterally, than
pain-free controls [5]. A less extended wrist might decrease
the tension of the finger flexor tendons, slowing the rate at
which the finger flexors can generate force output, thus
slowing the speed at which grip force can be achieved.
Earlier activation of ECR might also explain the increase in
latency between the onset of ECR EMG and the activation
of grip force in individuals with LE [20]. Previous work
during single-handed tennis strokes has revealed earlier
onset of ECRB than pain-free controls [15]. Whether such a
change reflects a positive adaptation or maladaptive
response is unclear. Earlier activation of ECR in the LE
group might be a purposeful strategy to compensate for a
compromised function of the ECRB muscle [26] and/or
tendon [2729]. Previous histological work has revealed
moth-eaten and necrotic muscle fibres in the symptomatic
ECRB muscle [26], and greater proportion of immature
tenocytes and neovascularisation of the symptomatic tendon
[29] of individuals with LE. Alternatively, changes in
forearm muscle activity might be influenced by regions
higher up the kinetic chain (e.g. shoulder, cervical/thoracic
spine). Although previous work has shown a higher presence
of cervical and thoracic pain in individuals with lateral
elbow pain compared with controls [30], further research is
required to investigate whether this has an impact on fore-
arm muscle activity. Although identification of differences
in the asymptomatic arm might represent a widespread
involvement of the CNS, further investigation is required.
Due to the case-control study design, it is not possible to
determine if changes in the temporal activation of forearm
muscles in individuals with LE are related to the devel-
opment of LE, or as a consequence of LE. Longitudinal
studies are required to investigate whether motor system
impairments are related to the cause of LE.
4.1.2 Tennis Strokes
A greater [19] and earlier [15] activity of forearm muscles
in individuals with LE than in pain-free controls during
tennis strokes might be explained by several possible
differences and could be related to either the cause or
effect of LE. First, individuals with LE might have a
modified afferent input or altered perception of the task.
Previous work has shown that LE is associated with a
reduced acuity of elbow proprioception than that observed
in pain-free controls [31]. In support, individuals with
rotator cuff tendinopathy consistently over estimated force
relative to pain-free controls (who consistently underes-
timated force) when asked to contract to a set force
without visual feedback [32]. It is possible that a greater
EMG activity and earlier activation of forearm muscles is
due to an overestimation or altered afferent input dis-
torting the required motor control. Second, it is possible
123
L. J. Heales et al.
that a greater EMG activation during tennis strokes in
individuals with LE might be explained by differences in
skill level, as previous work has suggested unskilled
tennis players often grip the tennis racquet too forcefully
[33]. As participants in the LE group in the study by
Kelley et al. [19] were level B and C recreational club
tennis players, and pain-free controls were either current
or former professional or division one collegiate tennis
players [19], the lower skill of the LE group may explain
their greater forearm muscle EMG amplitude. Third,
EMG analysis as a proportion of MVC requires consid-
eration as individuals with chronic pain conditions often
do not perform a true maximum contraction for reasons
including pain and fear of pain [25]. Use of an effort
lower than maximum for EMG normalisation would lead
to overestimation of EMG amplitude in the experimental
task, and this may explain the augmented activation of
multiple wrist extensor muscles.
Evidence of a greater [19] and earlier [15] activity of the
wrist extensor muscles (e.g. ECRB) in the LE group might
contribute to the development of LE, as this condition is
thought to be caused by an overuse of the forearm extensor
muscles, particularly the ECRB [29, 3437]. Additionally,
a tighter tennis racquet grip can induce greater vibrations if
the ball is not hit in the middle of the racquet [33]. Video
recordings from Kelley et al. [19] showed individuals with
LE consistently missed the centre of the racquet (5 of 8
[63 %] participants). Whether the combination of mis-hit-
ting and excessive grip force [33] contribute to the devel-
opment of LE requires further investigation.
With respect to differences in forearm muscle activity
during tennis strokes as a consequence of LE, modified
coordination of forearm muscles might be mediated by a host
of potential mechanisms. Greater activity of the wrist extensor
muscles in LE during tennis strokes might represent a
guarding response with the aim to limit pain provocation.
This is similar to the protective activation observed for some
muscles in other musculoskeletal conditions [38, 39].
Although such muscle guarding might be a positive adaption
in the presence of acute pain to reduce pain and injury, it could
lead to persistent changes in biomechanics [40] and further
pain/injury if maintained. Additionally, it is possible that
differences in the amplitude and timing of muscle activity
might be related to changes within the muscle. For example,
recent studies have identified a strong relationship between
inflammatory response and muscle changes following back
injuries in animals [41, 42]. Evans et al. [43] identified
inflammatory markers (e.g. interleukin-1 [IL-1]) in untrained
individuals after exercise. In addition, Ljung et al. [26] iden-
tified a greater presence of type 2A muscle fibres (fast twitch)
in individuals with LE than in pain-free controls. These
changes might alter the recording of action potentials but this
requires further investigation.
Forearm Muscle Activity in Lateral Epicondylalgia
4.1.3 Transcranial Magnetic Stimulation
Although this review identified two studies using TMS to
investigate corticomotor measures, only one revealed evi-
dence of cortical differences between individuals with LE
and pain-free controls using our a priori defined analysis
[16, 18]. Schabrun et al. [18] highlighted an absence of the
discrete cortical organisation of forearm muscles (ECRB
and EDC) in individuals with LE that was identified in
pain-free controls. This was reflected in fewer peaks of
excitability in the cortical map, and less distance between
the centres of gravity of ECRB and EDC in the LE group
than in the pain-free control group [18]. This finding is
similar to the observation that individuals with chronic low
back pain have less distance between the motor cortex
representation of different components of the lumbar
extensor muscles than pain-free controls [44]. Recent work
has shown changes in cortical areas, including the primary
motor cortex [45], that relate to modified motor behaviour
of individuals with chronic musculoskeletal pain. Whether
these changes are present prior to development of pain
(possibly even as a contributor), or whether these changes
occur after the development of pain, remains unknown and
longitudinal studies are required.
4.2 Interpretation of Features of Forearm Muscle
Activity That Do Not Differ in Lateral
Epicondylalgia
Identification of features that do not differ significantly
between groups is just as important as identifying those
that do. Such features give clinicians and researchers
insight into the similarities between individuals with LE
and pain-free controls. No studies identified statistical
differences between individuals with and without LE in
parameters of EMG median frequency (surrogate for
muscle fatigue) during gripping [6], EDC EMG amplitude
during tennis strokes [19], and features of corticomotor
excitability as tested by TMS [16, 18].
Absence of significant differences in median fre-
quency during gripping between those with and without
LE is interpreted to reflect a lack of between-group
differences in muscle fatigability. EMG median fre-
quency decreases during fatiguing tasks [46], and was
similar for LE and control groups in the study by Ali-
zadehkhaiyat et al. [6].
EDC has been suggested to be the source of symptoms
for individuals with LE [47]. Although the EDC muscle
primarily acts as a finger extensor [48], previous work has
shown that it is activated during gripping [24]. According
to the findings of Kelley et al. [19], EDC was activated
during tennis strokes in both groups (LE and controls) and
this activity did not differ between groups. This does not
1843
preclude differences in EDC for other measures, as has
been suggested by Schabrun et al. [18].
Analysis using our a priori criterion for SMD and
95 % CI did not identify any significant differences for
TMS measures of corticomotor excitability [16, 18].
This contrasts with the analysis outcome of Schabrun
et al. [18], who identified a significantly greater MEP
amplitude for ECRB and EDC in individuals with LE
than in pain-free controls, using an analysis of variance.
Our more lenient analysis method revealed this differ-
ence to be nearly significant. Schabrun et al. [18]
proposed that reduced cortical inhibition may account
for the greater MEP amplitude in individuals with LE.
This was based on evidence that intracortical inhibition
is reduced in chronic pain conditions [49]. The differ-
ence in outcome of analysis methods may be resolved by
inclusion of a larger number of participants in future
studies.
4.3 Clinical Implications
This systematic review highlights differences in forearm
muscle activity between individuals with LE and pain-free
controls that present as potentially modifiable factors that
may contribute to the efficacy of rehabilitation. Increas-
ingly, the treatment of tendinopathies like LE is targeted
towards motor function as well as pain relief with an
acknowledgement that there might be subgroups who will
require different combinations of approaches targeted at
pain or function [50]. Advice and education (e.g. activity
modification) and exercises targeted towards correcting
altered forearm muscle activity are possible candidate
targets to aid resolution of pain and functional issues, and
potentially reduce recurrence rates. Possible targets for
treatment could include education for tennis players
regarding gripping and ball hitting (e.g. ball in the centre of
the racquet strings), rehabilitation of kinematics and mus-
cle activation during wrist extension, and focus on inde-
pendent activation of ECRB and EDC. Such modifications
to treatment require investigation in clinical trials before
integration into practice.
4.4 Quality Assessment and Considerations
Interpretation of the findings of this review requires con-
sideration of several methodological issues. Meta-analysis
was not possible due to heterogeneity between tasks and
outcomes used in the included studies. The methodological
quality of the included studies was limited when assessed
using the EAI tool, with scores between 0.24 and 0.76
(mean 0.39) out of a possible 1. A major limitation was the
inability to determine the reliability and validity of the
outcome measures. Only one out of the seven (14 %)
123
1844
studies highlighted the lack of evidence of validity and
reliability of the neuromuscular control technique as a
limitation of the study [18]. Only one study (14 %) men-
tioned other limitations which may affect their generalis-
ability [20].
5 Conclusion
This review highlights the limited and heterogeneous nat-
ure of research regarding forearm muscle activity in LE.
This review identified evidence of differences in forearm
muscle activity (recorded with EMG) between individuals
with LE and pain-free controls, but differences in the
methods make it impossible to draw robust conclusions.
Further studies are required with larger sample sizes and
consistent methodologies to allow for meta-analysis. Evi-
dence of altered temporal parameters in the asymptomatic
limb of individuals with unilateral LE may indicate more
widespread motor changes, but further investigation is
required.
Compliance with Ethical Standards
Funding Funding for this work was provided by a Program Grant
from the National Health and Medical Research Council (NHMRC)
of Australia (ID631717). Paul Hodges is supported by a Senior
Principal Research Fellowship (APP1002190) and Luke Heales by an
Australian Postgraduate Award scholarship.
Conflicts of interest Luke Heales, Michael Bergin, Bill Vicenzino
and Paul Hodges declare that they have no conflicts of interest rele-
vant to the content of this review.
References
1. Lim ECW. Pain free grip strength test. J Physiother. 2013;59
(1):59.
2. Coombes B, Bisset L, Vicenzino B. A new integrative model of
lateral epicondylalgia. Br J Sports Med. 2009;43:2528. doi:10.
113/bjsm.2008.052738.
3. Priest JD, Jones HH, Nagel DA. Elbow injuries in highly skilled
tennis players. J Sports Med. 1974;2(3):139.
4. Silverstein B, Viikari-Juntura E, Kalat J. Use of a prevention
index to identify industries at high risk for work-related muscu-
loskeletal disorders of the neck, back, and upper extremity in
Washington State, 19901998. Am J Ind Med. 2002;41(3):149
69.
5. Bisset LM, Russell T, Bradley S, et al. Bilateral sensorimotor
abnormalities in unilateral lateral epicondylalgia. Arch Phys Med
Rehabil. 2006;87(4):4905. doi:10.1016/j.apmr.2005.11.029.
6. Alizadehkhaiyat O, Fisher A, Kemp G, et al. Upper limb muscle
imbalance in tennis elbow: a functional and electromyographic
assessment. J Orthop Res. 2007;25(12):16517. doi:10.1002/jor.
20458.
7. Skinner DK, Curwin SL. Assessment of fine motor control in
patients with occupation-related lateral epicondylitis. Man Ther.
2007;12(3):24955.
123
L. J. Heales et al.
8. Pienimaki T, Kauranen K, Vanharanta H. Bilaterally decreased
motor performance of arms in patients with chronic tennis elbow.
Arch Phys Med Rehabil. 1997;78(10):10925.
9. Konrad P. The ABC of EMG: A practical introduction to kine-
siological electromyography. USA: Noraxon USA Inc; 2005.
10. Rudroff T. Kinesiological fine wire EMG: A practical introduction
to fine wire EMG applications. USA: Noraxon USA Inc; 2008.
11. Genaidy AM, LeMasters GK, Lockey J, et al. An epidemiological
appraisal instrumenta tool for evaluation of epidemiological
studies. Ergonomics. 2007;50(6):92060. doi:10.1080/
00140130701237667.
12. Landis JR, Koch G. The measurement of observer agreement for
categorical data. Biometrics. 1977;33(1):15974. doi:10.2307/
2529310.
13. Cohen J. Statistical power analysis for the behavioral sciences.
2nd ed. Hillsdale: Erlbaum; 1988.
14. Lim ECW, Sterling M, Pedler A, et al. Evidence of spinal cord
hyperexcitability as measured with nociceptive flexion reflex
(NFR) threshold in chronic lateral epicondylalgia with or without
a positive neurodynamic test. J Pain. 2012;13(7):67684.
15. Bauer JA, Murray RD. Electromyographic patterns of individuals
suffering from lateral tennis elbow. J Electromyogr Kinesiol.
1999;9(4):24552.
16. Dessureault L, Tremblay F, Bilodeau M. Corticomotor
excitability and proprioceptive acuity in chronic lateral epi-
condylalgia [Thesis]. Ottawa: University of Ottawa; 2008.
17. Calder KM, Stashuk DW, McLean L. Motor unit potential morphol-
ogy differences in individuals with non-specific arm pain and lateral
epicondylitis. J Neuroeng Rehabil. 2008;5(December):Article 34.
18. Schabrun SM, Hodges PW, Vicenzino B, et al. Novel adaptations
in motor cortical maps: The relationship to persistent elbow pain.
Med Sci Sports Exerc. 2014;47(4):68190.
19. Kelley JD, Lombardo SJ, Pink M, et al. Electromyographic and
cinematographic analysis of elbow function in tennis players with
lateral epicondylitis. Am J Sports Med. 1994;22(3):35963.
20. Chourasia AO, Buhr KA, Rabago DP, et al. Effect of lateral
epicondylosis on grip force development. J Hand Surg Am.
2012;25(1):2737. doi:10.1016/j.jht.2011.09.003.
21. Roos MR, Rice CL, Vandervoort AA. Age-related changes in
motor unit function. Muscle Nerve. 1997;20(6):67990.
22. Linnamo V, Moritani T, Nicol C, et al. Motor unit activation pat-
terns during isometric, concentric and eccentric actions at different
force levels. J Electromyogr Kinesiol. 2003;13(1):93101.
23. Georgoulis AD, Ristanis S, Papadonikolakis A, et al. Elec-
tromechanical delay of the knee extensor muscles is not altered
after harvesting the patellar tendon as a graft for ACL recon-
struction: Implications for sports performance. Knee Surg Sports
Traumatol Arthrosc. 2005;13:43743.
24. Snijders CJ, Volkers AC, Mechelse K, et al. Provocation of
epicondylalgia lateralis (tennis elbow) by power grip or pinching.
Med Sci Sports Exerc. 1987;19(5):51823.
25. Lindstroem R, Graven-Nielsen T, Falla D. Current pain and fear
of pain contribute to reduced maximum voluntary contraction of
neck muscles in patients with chronic neck pain. Arch Phys Med
Rehabil. 2012;93(11):20428.
26. Ljung BO, Lieber RL, Friden J. Wrist extensor muscle pathology
in lateral epicondylitis. J Hand Surg Am. 1999;24B(2):17783.
27. Levin D, Nazarian LN, Miller TT, et al. Lateral epicondylitis of
the elbow: US findings. Radiology. 2005;237(1):2304.
28. Heales LJ, Broadhurst N, Mellor R, et al. Diagnostic ultrasound
imaging for lateral epicondylalgia: a case control study. Med Sci
Sports Exerc. 2014;46(11):20706. doi:10.1249/MSS.
0000000000000345.
29. Nirschl RP. Elbow tendinosis/tennis elbow. Clin Sports Med.
1992;11(4):85170.
Forearm Muscle Activity in Lateral Epicondylalgia
30. Berglund KM, Persson BH, Denison E. Prevalence of pain and
dysfunction in the cervical and thoracic spine in persons with and
without lateral elbow pain. Man Ther. 2008;13(4):2959. doi:10.
1016/j.math.2007.01.015.
31. Juul-Kristensen B, Lund H, Hansen K, et al. Poorer elbow pro-
prioception in patients with lateral epicondylitis than in healthy
controls: a cross-sectional study. J Shoulder Elbow Surg. 2008;17
(1 SUPPL.):S7281.
32. Maenhout AG, Palmans T, De Muynck M, et al. The impact of
rotator cuff tendinopathy on proprioception, measuring force
sensation. J Shoulder Elbow Surg. 2012;21(8):10806.
33. Hatze H. Forces and duration of impact, and grip tightness during
the tennis stroke. Med Sci Sports Exerc. 1976;8(2):8895.
34. Nirschl RP, Ashman ES. Elbow tendinopathy: tennis elbow. Clin
Sports Med. 2003;22(4):81336. doi:10.1016/S0278-5919(03)
00051-6.
35. Nirschl RP, Ashman ES. Tennis elbow tendinosis (epicondylitis).
Instr Course Lect. 2004;53:58798.
36. Budoff JE, Nirschl RP. Resection and repair of lateral tennis
elbow. Oper Tech Sports Med. 2001;9(4):2116.
37. Marx RG, Sperling JW, Cordasco FA. Overuse injuries of the
upper extremity in tennis players. Clin Sports Med. 2001;20
(3):43951.
38. Arendt-Nielsen L, Graven-Nielsen T, Svarrer H, et al. The
influence of low back pain on muscle activity and coordination
during gait: a clinical and experimental study. Pain. 1996;64
(2):23140. doi:10.1016/0304-3959(95)00115-8.
39. van der Hulst M, Vollenbroek-Hutten MM, Rietman JS, et al.
Lumbar and abdominal muscle activity during walking in sub-
jects with chronic low back pain: Support of the guarding
hypothesis? J Electromyogr Kinesiol. 2010;20(1):318. doi:10.
1016/j.jelekin.2009.03.009.
40. Verbunt JA, Seelen HA, Vlaeyen JW, et al. Disuse and decon-
ditioning in chronic low back pain: concepts and hypotheses on
contributing mechanisms. Eur J Pain. 2003;7(1):921. doi:10.
1016/S1090-3801(02)00071-X.
1845
41. Hodges PW, James G, Blomster L, et al. Can proinflammatory
cytokine gene expression explain multifidus muscle fiber changes
after an intervertebral disc lesion? Spine. 2014;39(13):10107.
doi:10.1097/BRS.0000000000000318.
42. Hodges PW, James G, Blomster L, et al. Multifidus muscle
changes after back injury are characterized by structural remod-
eling of muscle, adipose and connective tissue, but not muscle
atrophy: molecular and morphological evidence. Spine. 2015;40
(14):105771. doi:10.1097/BRS.0000000000000972.
43. Evans WJ, Meredith CN, Cannon JG, et al. Metabolic changes
following eccentric exercise in trained and untrained men. J Appl
Physiol. 1986;61(5):18648.
44. Tsao H, Danneels LA, Hodges PW. ISSLS prize winner:
smudging the motor brain in young adults with recurrent low
back pain. Spine. 2011;36(21):17217.
45. Pelletier R, Higgins J, Bourbonnais D. Is neuroplasticity in the
central nervous system the missing link to our understanding of
chronic musculoskeletal disorders? BMC Musculoskelet Disord.
2015;16:25. doi:10.1186/s12891-015-0480-y.
46. Lowery MM, OMalley MJ. Analysis and simulation of changes
in EMG amplitude during high-level fatiguing contractions. IEEE
Trans Biomed Eng. 2003;50(9):105262.
47. Fairbank SM, Corlett RJ. The role of the extensor digitorum
communis muscle in lateral epicondylalitis. J Hand Surg Br.
2002;27(5):4059. doi:10.1054/jhsb.2002.0761.
48. Saladin KS. Human Anatomy. 3rd ed. New York: McGraw Hill;
2011.
49. Lefaucheur JP, Drouot X, Menard-Lefaucheur I, et al. Motor
cortex rTMS restores defective intracortical inhibition in chronic
neuropathic pain. Neurology. 2006;67(9):156874.
50. Coombes BK, Bisset L, Vicenzino B. Management of lateral
elbow tendinopathy: one size does not fit all. J Orthop Sports
Phys Ther. 2015;45(11):93849. doi:10.2519/jospt.2015.5841.
123