ORIGINAL RESEARCH
published: 07 February 2017
doi: 10.3389/fphys.2017.00026
No Influence of Transcutaneous
Electrical Nerve Stimulation on
Exercise-Induced Pain and 5-Km
Cycling Time-Trial Performance
Andrew W. Hibbert 1, 2*, François Billaut 1, 3 , Matthew C. Varley 1 and Remco C. J. Polman 1, 4
1
Institute of Sport, Exercise, and Active Living, Victoria University, Melbourne, VIC, Australia, 2 College of Sport and Exercise
Science, Victoria University, Melbourne, VIC, Australia, 3 Department of Kinesiology, University Laval, Quebec, QC, Canada,
4
Psychology Department, Bournemouth University, Bournemouth, UK
Edited by:
Alexis R. Mauger,
University of Kent, UK
Reviewed by:
Pascal Edouard,
University Hospital of Saint-Etienne,
France
Stephane Perrey,
University of Montpellier, France
Martyn Morris,
Coventry University, UK
*Correspondence:
Andrew W. Hibbert
andrew.hibbert1@live.vu.edu.au
Specialty section:
This article was submitted to
Exercise Physiology,
a section of the journal
Frontiers in Physiology
Received: 14 September 2016
Accepted: 11 January 2017
Published: 07 February 2017
Citation:
Hibbert AW, Billaut F, Varley MC and
Polman RCJ (2017) No Influence of
Transcutaneous Electrical Nerve
Stimulation on Exercise-Induced Pain
and 5-Km Cycling Time-Trial
Performance. Front. Physiol. 8:26.
doi: 10.3389/fphys.2017.00026
Frontiers in Physiology | www.frontiersin.org
Introduction: Afferent information from exercising muscle contributes to the sensation
of exercise-induced muscle pain. Transcutaneous electrical nerve stimulation (TENS)
delivers low–voltage electrical currents to the skin, inhibiting nociceptive afferent
information. The use of TENS in reducing perceptions of exercise-induced pain has
not yet been fully explored. This study aimed to investigate the effect of TENS on
exercise-induced muscle pain, pacing strategy, and performance during a 5-km cycling
time trial (TT).
Methods: On three separate occasions, in a single-blind, randomized, and cross-over
design, 13 recreationally active participants underwent a 30-min TENS protocol, before
performing a 5-km cycling TT. TENS was applied to the quadriceps prior to exercise
under the following conditions; control (CONT), placebo with sham TENS application
(PLAC), and an experimental condition with TENS application (TENS). Quadriceps fatigue
was assessed with magnetic femoral nerve stimulation assessing changes in potentiated
quadriceps twitch force at baseline, pre and post exercise. Subjective scores of exertion,
affect and pain were taken every 1-km.
Results: During TTs, application of TENS did not influence pain perceptions (P = 0.68,
η2p = 0.03). There was no significant change in mean power (P = 0.16, η2p = 0.16) or TT
duration (P = 0.17, η2p = 0.14), although effect sizes were large for these two variables.
Changes in power output were not significant but showed moderate effect sizes at 500-m
(η2p = 0.10) and 750-m (η2p = 0.10). Muscle recruitment as inferred by electromyography
data was not significant, but showed large effect sizes at 250-m (η2p = 0.16), 500-m
(η2p = 0.15), and 750-m (η2p = 0.14). This indicates a possible effect for TENS influencing
performance up to 1-km.
Discussion: These findings do not support the use of TENS to improve 5-km TT
performance.
Keywords: transcutaneous electrical nerve stimulation, pacing, performance, afferent feedback, time-trial
1
February 2017 | Volume 8 | Article 26
Hibbert et al.
TENS and Exercise
INTRODUCTION
intensity (and possibly performance), before perceptions become
prominent.
An alternative to ingested and injected analgesics is
transcutaneous electrical nerve stimulation (TENS). Application
of TENS involves low-voltage electrical currents administered
to the skin for pain relief (Johnson et al., 2015). Analgesic
effects are provided following the gate control theory of pain
(Melzack and Wall, 1965), which controls transmission of
nociceptive information. Specifically, stimulation provided by
TENS targeting group II muscle afferent fibers excites inhibitory
interneurons. This results in an attenuation of the ascending
nociceptive stimuli from group III and IV afferent fibers (Sluka
et al., 2013; Johnson et al., 2015). Based on this premise, it is
possible that TENS could be used to attenuate nociceptive stimuli
associated with aerobic exercise. Clinically, analgesic effects of
TENS have been demonstrated for chronic musculoskeletal
pain (Johnson and Martinson, 2007). In pain-free individuals,
application can influence pressure pain thresholds (PPT).
(Moran et al., 2011). During exercise in pain-free individuals,
TENS application has improved tolerance by enhancing
peripheral blood flow (Tomasi et al., 2015). Furthermore,
when knee pain was induced, TENS has also reduced pain and
restored quadriceps strength (Son et al., 2016). This suggests
that TENS could be used in pain-free individuals to reduce
pain perceptions, and possibly perceptions of exercise-induced
pain. If demonstrated, a reduction of exercise-induced pain,
in conjunction with possible alterations in muscle contractile
properties and enhancement of blood flow, gives the potential
for TENS application to be a performance enhancing strategy.
To the authors’ knowledge, TENS has not been used
in pain-free participants to modulate afferent feedback and
reduce exercise-induced pain perceptions during self-paced
exercise. Based on the potential to influence exercise-induced
pain, the aim of this study was to investigate the efficacy
of TENS administered before intense exercise to influence
pain perceptions. It was hypothesized that TENS would
influence the threshold for sensing exercise-induced pain,
thereby increasing exercise intensity and performance for similar
subjective pain perceptions. As TENS can influence muscle
excitability and strength, a secondary objective was to assess
within-exercise muscle recruitment (via electromyography) and
neuromuscular fatigue. To allow the assessment of muscle
recruitment, application of TENS was administered prior to
exercise, in anticipation of approximately 30-min of poststimulation analgesia, utilizing similar TENS settings displaying
increased PPT within this period (Moran et al., 2011;
Pantaleão et al., 2011). To allow for exercise to be within
the post-stimulation time frame, a 5-km cycling TT was
utilized, as it was anticipated this would be completed in
∼10-min.
Pacing is the regulation of effort during exercise that aims
to manage neuromuscular fatigue. It prevents excessive
physiological harm and maximizes goal achievement (Edwards
and Polman, 2013). To accomplish this, decisions are made
based on information received from both internal, and external
environments, to adjust exercise intensity (Edwards and Polman,
2013; Smits et al., 2014). Initially, pacing strategies are set in
anticipation (Ulmer, 1996; Tucker, 2009), whilst regulation of
intensity during exercise is influenced by afferent information
from exercising muscle (Amann et al., 2009). Therefore, the
ability to adjust or remove this information is of interest in
pacing research, as there is potential to improve performance.
Exercise typically augments mechanical and chemical stimuli
within the muscle, sensitizing, and activating nociceptive
group III and IV afferent muscle fibers. These communicate
information on actual or potential muscle damage to the
central nervous system (O’Connor and Cook, 1999). Conscious
awareness of this information forms the subjective sensation
of exercise-induced pain (Loeser and Treede, 2008; Mauger,
2013). Pacing theory states that low signal (feedback) intensity
will not trigger awareness (Swart et al., 2012). Yet, with an
increasing stimulus intensity (i.e., intense exercise), conscious
awareness is achieved, which results in appropriate decisions
to change behavior (Swart et al., 2012; Edwards and Polman,
2013). Therefore, once nociceptive signals and consequently
perceptions of pain become prominent, effort will be regulated
to maintain discomfort at a tolerable level (Swart et al., 2012;
Edwards and Polman, 2013; Mauger, 2014). This concept of
a “sensory tolerance limit” (Gandevia, 2001; Hureau et al.,
2016), likely occurs to prevent excessive physiological harm
by limiting levels of fatigue (Amann et al., 2009). The sum
of signals from a number of mechanisms contribute to this
theory, including feedback from group III and IV muscle
afferents but also feedback from respiratory muscles and
corollary discharges (Hureau et al., 2016). Reductions to exercise
performance and duration due to exercise-induced fatigue, are
evidence of this concept (Amann et al., 2013). In addition,
the importance of nociceptive information as part of a global
tolerance limit has been demonstrated by altered nociceptive
stimuli (i.e., induced or blocked), leading to changes in voluntary
activation of muscle (Amann et al., 2009; Kennedy et al.,
2014). Only a small number of studies, investigating analgesic
interventions to augment afferent information have focused on
exercise pacing and performance. Injecting fentanyl increases
initial power output, but results in excessive fatigue (Amann
et al., 2009), while ingestion of acetaminophen can increase
mean power output during a time trial (TT) (Mauger et al.,
2010) and during repeated-sprint exercise (Foster et al., 2014).
An increased exercise intensity suggests nociceptive signals
affect self-pacing. Yet, in acetaminophen studies, there was
no change in pain perceptions. This suggests a threshold
of perceived pain was adjusted and exercise intensity was
increased to this tolerance limit. Therefore, there is merit for
any analgesic intervention during self-paced exercise to adjust
perceptions of exercise-induced pain allowing for an increased
Frontiers in Physiology | www.frontiersin.org
METHODS
Participants
Thirteen recreationally active participants were recruited for this
study (see Table 1). Written informed consent was provided in
accordance with the Declaration of Helsinki. The inclusion of
2
February 2017 | Volume 8 | Article 26
Hibbert et al.
TENS and Exercise
before PRE measurement of MVC. Immediately following
PRE measurements, a 5-s sprint was conducted for EMG
normalization purposes. Following this, the TT commenced
after a verbal 3-s countdown from the researcher. To overcome
flywheel inertia, participants were instructed to obtain a selfselected comfortable cadence immediately prior to beginning
the TT. All exercise was conducted on a Velotron Pro cycle
ergometer (RacerMate Inc., Seattle, WA, USA). Within the
familiarization sessions, participants set the ergometer to their
own specifications with values recorded and replicated for
subsequent sessions. All TT protocols were controlled via
Velotron Coaching software (Version 1.6.458, RacerMate Inc.)
with all courses being flat with no wind effect. Participants were
permitted to drink water ad libitum during trials. Participants
were instructed to finish the required distance “as quickly as
possible,” being free to change gear and cadence throughout the
TT as desired. Participants were blinded from information except
for distance covered. Upon TT completion, participants were
quickly assisted in moving to the MVC and magnetic stimulation
apparatus, for POST assessment.
TABLE 1 | Participant anthropometric data.
Female
Male
Total
n=4
n=9
n = 13
Age (years)
27.5 ± 7.4
23.3 ± 4.2
24.6 ± 5.5
Height (cm)
166.0 ± 9.1
179.5 ± 7.0
175.3 ± 9.8
Body mass (kg)
62.2 ± 9.2
77.1 ± 7.8
72.8 ± 10.6
250.3 ± 39.7
321.3 ± 23.0
299.5 ± 43.7
PPO (W/kg)
4.0 ± 0.4
4.2 ± 0.5
4.2 ± 0.5
VO2peak (L.min−1 )
2.6 ± 0.6
3.8 ± 0.3
3.4 ± 0.7
40.9 ± 6.3
49.4 ± 5.6
46.7 ± 6.9
7.8 ± 2.9
9.0 ± 1.1
8.6 ± 1.8
PPO (W)
VO2peak (ml.min.kg−1 )
Pain at PPO
Data presented as mean ± SD. PPO, peak power output; VO2peak , peak oxygen
consumption; Pain at PPO, rating of perceived quadriceps pain at PPO.
both males and females was based on indications sex has no
influence on level of exercise-induced pain within the time frame
proposed for this study (Dannecker et al., 2012), with repeated
measures trial design minimizing any potential differences. Using
a medical questionnaire, all participants were screened for
risk factors including suitability to the exercise, current pain,
currently taking pain medication and any prior use of TENS.
Participants who reported pain (chronic or acute) or prior use
of TENS were excluded from the study. Participants were asked
to refrain from any physical activity causing severe fatigue in the
36 h prior, as well as any caffeine intake or pain medication 2 h
prior to testing sessions. Procedures were approved by Victoria
University’s Human Research Ethics Committee.
VO2 Assessment
After TT familiarization sessions, to characterize participants,
VO2peak was assessed via a maximal incremental test. A ramp
protocol was utilized, that equated to 30 Watts/min which
commenced after a 3-min baseline period, cycling at 0 Watts
(Vanhatalo et al., 2007). As participant familiarity with cycling
varied, a similar test was chosen to that used for participants
unfamiliar with cycling (Williams et al., 2012). Expired gas was
collected and analyzed every 15-s (S-3A/I (O2) and CD-3A
(CO2), AEI Technologies Inc., Pittsburgh, PA). Prior to each
test, gases were calibrated with known concentrations and flow
calibrations were performed using a 3-L calibration syringe.
Participants were encouraged throughout the final stages and the
test ceased when the participant could not maintain a cadence
above 60 rpm or volitional fatigue was achieved. Peak oxygen
uptake was calculated as the highest 30-s mean VO2 and peak
power defined as the highest power at test conclusion. Subjective
ratings for exertion (RPE) and quadriceps pain (pain scale) were
measured every minute.
Experimental Procedures
Participants reported to the laboratory for seven sessions, which
included four preliminary and three experimental sessions.
Prior to experimental sessions, three 5-km TT sessions were
conducted to familiarize participants and ensure adequate
reliability of pacing and performance (Hibbert et al., unpublished
data). Furthermore, during the first session participants were
also familiarized with TENS, peripheral magnetic stimulation
protocols and algometry (see procedures below). The final
preliminary session was a peak oxygen uptake (VO2peak )
assessment to characterize participants’ cardiorespiratory fitness.
For experimental testing, on three different days separated by a
minimum of 48 h, participants performed three 5-km cycling TTs
in a single-blind randomized order: control (CONT), placebo
with sham TENS application (PLAC), and an experimental
condition with TENS application (TENS). TENS was applied for
30-min before performing a cycling TT (see TENS procedure
below). Maximal voluntary contraction (MVC) force, responses
to magnetic stimulation of the quadriceps and PPT were
measured before TENS application (BASE), as well as pre (PRE),
and immediately post (POST) exercise.
Upon reporting to the laboratory, participants were fitted
with electromyography (EMG) electrodes (see below). A warm
up of MVC and magnetic stimulation (see below) was
conducted before BASE measurement. Participants were then
fitted with TENS electrodes for 30-min of TENS application.
A cycling warm-up (5-min cycling at 75 Watts) was conducted
Frontiers in Physiology | www.frontiersin.org
Transcutaneous Electrical Nerve
Stimulation (TENS)
Participants were acutely treated with TENS (N602 ProTens;
Everyway Medical Instruments, New Taipei City, Taiwan) for 30min prior to the exercise protocol. Two TENS units were used
so that the area of stimulation could be increased, with one unit
(two channels) dedicated to each leg. Stimulation was applied
through 50 × 90 mm adhesive electrodes (Allcare; Everyway
Medical Instruments, New Taipei City, Taiwan). TENS electrode
placement occurred after BASE MVC measurement, with sites
shaved before placement. At the conclusion of stimulation, TENS
electrodes were removed. For electrode placement, participants
were asked to lay in a supine position and perform a knee
extension. Two electrodes were placed on the superior portion
of the quadriceps, inferior to the inguinal fold over the areas
of contracted muscle bulk. Two electrodes were also placed
3
February 2017 | Volume 8 | Article 26
Hibbert et al.
TENS and Exercise
for individual muscles was analyzed for 20-s at 250-m intervals
of TT distance. Individual muscle RMS values were summed to
estimate general muscle electrical activity (RMSsum ) (Billaut et al.,
2010), and is reported as a percent of the individual maximum
value obtained during a pre-exercise sprint (O’Bryan et al., 2014).
over the inferior portion of the quadriceps, one over the vastus
lateralis and one over the vastus medialis. TENS was delivered
in constant mode with settings fixed at a pulse width of 200µs, and frequency of 82.6-Hz (Chen and Johnson, 2010). The
duration and settings (pulse width and frequency) of TENS was
based on previous studies showing the effect of TENS on PPT
(Moran et al., 2011; Pantaleão et al., 2011). In this investigation,
for the assessment of muscle recruitment and practically of
exercise, application of TENS was administered prior to exercise
in anticipation of approximately 30-min of post-stimulation
analgesia (i.e., increased PPT) as observed in previous studies
(Moran et al., 2011; Pantaleão et al., 2011). Prior to study
commencement, settings for the TENS units were verified using
an oscilloscope (Rigol DS1054). Following calibration checks,
transparent tape was placed over these controls to prevent any
adjustment. For TENS application, participants were instructed
to adjust intensity (via manual dials) to a level of non-painful
tingling below a level that evokes involuntary muscle contraction
(Moran et al., 2011; Pantaleão et al., 2011; Son et al., 2016).
Throughout 30-min TENS application, participants were asked
to periodically increase intensity to ensure this remained at
desired level. For PLAC condition, the same electrode placement
was used, but stimulation intensity was set by the researcher.
To appear that stimulation was present, the TENS unit power
indicator was illuminated, although the equipment did not
provide stimulation. For this condition, participants were told
stimulation was set to a sub-sensory level (Cheing et al., 2002).
For TENS condition, participants were informed that they were
receiving high TENS and low TENS for PLAC condition. In
both conditions, participants were advised that they may or
may not feel any stimulation and in the absence of sensation,
stimulation was still active and providing analgesic effects. To
account for time taken for TENS application, during CONT
condition, participants laid quietly in a supine position for 30min.
Peripheral Magnetic Stimulation
Stimulation of the femoral nerve and quadriceps muscle was
conducted using a magnetic stimulator (Magstim RAPID2 ; JLM
Accutek Healthcare, Homebush, NSW) and a double 70-mm coil
(Katayama et al., 2004; Amann et al., 2007; Billaut et al., 2013).
Force responses were obtained at 1 kHz from a calibrated load
cell (Extran 2kN “S” beam, model SW1, Applied Measurement,
Melbourne, Australia). The load cell was connected to a noncompliant strap, which was attached around the participant’s
leg just superior to the malleoli of the ankle. Voluntary force
and neuromuscular testing was conducted at BASE, PRE (∼3min pre-exercise) and POST (between 40 and 60-s post-exercise).
Allowing for removal of TENS electrodes and application of
EMG electrodes, the delay between the end of TENS application
and PRE, was approximately 10-min. Time taken from the start
of PRE assessment to TT start was ∼6-min.
To determine the area of stimulation associated with the
largest quadriceps twitch (Qtw ), the coil head was positioned
high onto the thigh, between the quadriceps muscle and the
femoral triangle (Katayama et al., 2004; Amann et al., 2007;
Billaut et al., 2013). This position was marked and kept the
same for all trials. At BASE a warm-up was conducted with
brief (∼5-s) submaximal voluntary contractions increasing to a
MVC separated by ∼40-s. To indicate maximal depolarization
of the femoral nerve, a ramp protocol of increasing stimulus
intensity (from 70 to 100%) was used to achieve a plateau in
BASE Qtw (Katayama et al., 2004; Amann et al., 2007; Billaut
et al., 2013). A near plateau was achieved in all participants
at 95–100% stimulator output. For assessment, the stimulus
power was set at 100% of maximum, and single stimuli were
delivered. During a 5-s MVC of the quadriceps, the femoral nerve
was stimulated (superimposed single stimuli) to determine the
completeness of muscle activation (Katayama et al., 2004; Amann
et al., 2007; Billaut et al., 2013). Stimulation was administered
when the researcher visually identified a plateau in torque (Tofari
et al., 2016). Three potentiated quadriceps twitches (Qtw,pot ) were
obtained 5-s after the MVC. This procedure was performed three
times at BASE and PRE (60-s of rest in between) such that
nine Qtw,pot values were obtained, with the Qtw,pot averaged and
analyzed for peak force. The procedure was only performed once
at end-exercise to reduce post-exercise assessment time and limit
recovery as much as possible (Billaut et al., 2013). Surface EMG
was used to assess the membrane excitability via muscle action
potentials (M-waves) during potentiated twitches, with peak to
peak duration and amplitude measured. With single stimuli
delivered during the MVCs the quadriceps central activation
ratio (CAR) was calculated as the percentage of voluntary force
obtained during the superimposed contraction, that is, CAR =
MVC ÷ (MVC + stimulated force) (Kent-Braun, 1999; Tofari
et al., 2016). Stimulation was delivered on visual identification
of torque plateau, and in some cases, it occurred before or
Electromyography
Electromyographic (EMG) activity of six muscles (vastus
medialis, vastus lateralis, rectus femoris, biceps femoris, medial
gastrocnemius, and gluteus maximus) was recorded from the right
lower limb via Ag/AgCl bipolar rectangular electrodes with a
diameter of 30 × 20 mm and an inter-electrode distance of
20 mm (Blue Sensor N-00-S, Ambu Medicotest A/S, Ølstykke,
Denmark). All signals were recorded continuously at 1500 Hz
via a wireless receiver (Telemyo 2400 GT, Noraxon Inc., USA).
Prior to electrode placement, the limb was shaved and abraded to
minimize skin impedance, and appropriate electrode placement
and functionality was checked before the start of each test.
When the position of quadriceps electrodes overlapped with
TENS electrode placement, electrode location was marked with
a waterproof felt-tip pen to ensure reliable electrode replacement
within session. All electrode sites were marked for reliable
placement between subsequent testing sessions. To avoid artifacts
from lower-limb movements, the electrodes were well secured
with rigid tape. Raw EMG signals were band-pass filtered (12–
500 Hz), were full-wave rectified and Root Mean Squared using
Noraxon software (MyoResearch XP version 1.08.27). Mean RMS
Frontiers in Physiology | www.frontiersin.org
4
February 2017 | Volume 8 | Article 26
Hibbert et al.
TENS and Exercise
was violated, Greenhouse-Geisser correction was used to adjust
degrees of freedom. Paired samples t-tests were used to analyze
subjective ratings of the TENS. For a significant main effect,
post-hoc comparisons were examined with a one-way repeated
measures ANOVA with Sidak multiple comparisons and paired
sample t-tests. Statistical significance levels for all tests was set
at P < 0.05. Effect sizes for ANOVA are reported as partial eta
squared (η2p ) with a small effect at 0.01, medium effect 0.06 and a
large effect > 0.14. Effect sizes for t-tests are reported as Cohen’s
d with a small effect at 0.2, medium 0.5, and large >0.8 (Cohen,
1988).
after the torque plateau. To account for this, a correction
equation was used where torque was averaged over 100-ms before
superimposed peak (Marshall et al., 2014; Tofari et al., 2016). Due
to technical problems, some CAR data were not included, and
these participants have been removed from analysis with total
n = 10.
Perceptual Scores
A 6–20 scale of rated perceived exertion (RPE) (Borg, 1970),
an 11-point bipolar feeling scale (FS) (Hardy and Rejeski, 1989)
and a pain scale (O’Connor and Cook, 2001) were used to
assess perceived effort, affect and perceived quadriceps muscle
pain. Prior to commencing the study, participants were given
instructions and explained all scales. During familiarization and
experimental TTs, ratings were recorded at every kilometer.
At the conclusion of the study, participants were asked
to subjectively access the effectiveness of TENS application.
Participants were asked to rate on a 1–10 scale (1; a bit, 10; a
lot), the relief from pain, and impact on performance that TENS
application provided. Responses were received for both TENS
and PLAC conditions.
RESULTS
Perceptual Scores and Pain
There was a significant distance effect for RPE, FS and pain
(P < 0.01), with all conditions having an increase in RPE and
pain, whilst having a decrease in FS (Table 2). No significant
interaction (Condition × distance) effect was found for any
perceptual score, RPE (P = 0.58), FS (P = 0.68), and perceived
quadriceps pain (P = 0.68) (Table 2). However, FS showed a
moderate effect size and RPE had a large effect size for the
interaction and trial effects. There was also no change in pressure
pain thresholds attributed to TENS (see Tables 3, 4). Post study
subjective ratings of the effectiveness of TENS were different
between PLAC and TENS conditions for the level of pain relief
[t (12) = 2.68 P = 0.02, d = 1.55] and positive influence on
performance [t (12) = 4.68 P < 0.01, d = 2.70] (Figure 1) with
large effect sizes.
Algometer
Measures of PPT were recorded for the pressure applied to
the quadriceps with an algometer (FPX algometer; Wagner
Instruments) with a 1-cm2 application surface. Recordings
displayed in kilograms of force (kgf) were taken from the left
leg at BASE, in the last minute of TENS application (i.e., PRE
exercise) and at POST. Assessment site was the midpoint between
anterior superior iliac spine and head of the patella. Recordings
were taken with pressure applied to relaxed muscle at a rate
of 1 kg. cm−2. s−1 . Participants verbally reported the first point
when pain (distinct from pressure or discomfort) occurred,
the algometry was immediately removed and corresponding
measurement recorded as PPT (Moran et al., 2011).
Overall Performance
There was no significant difference for mean power maintained
over the TT [F (1.8, 21.8) = 2.0, P = 0.16, η2p = 0.16], although there
was a large effect size (Figure 2A). Completion time between
conditions was not significantly different [F (2, 24) = 1.9, P = 0.17,
η2p = 0.14] and had a large effect size (Figure 2C). Average power
for the first kilometer was not significantly different [F (1.4, 16.6)
= 1.8, P = 0.21, η2p = 0.13] (Figure 2B), as was duration
[F (1.8, 21.5) = 1.7, P = 0.20, η2p = 0.13] (Figure 2D), however both
had a moderate effect size. Visual inspection of data (Figure 2D)
shows a decreased time in TENS condition. Of all participants,
nine had a reduced time in the TENS condition at one kilometer
compared to CONT (−3.12 ± 5.58 s to CONT, 95% CI; −6.49,
0.26) (Figure 3D). For total TT duration eight out of 13 improved
their time in TENS compared to CONT (−3.82 ± 12.96 s to
CONT, 95% CI; −11.65, 4.01) (Figure 3C).
Statistical Analysis
Conditions are defined as control (CONT), placebo with sham
TENS application (PLAC), and an experimental condition with
TENS application (TENS). All data was analyzed using SPSS
(version 22, SPSS Inc., Chicago, IL.), with data are reported
as mean ± SD. Tests for homogeneity of variances were
performed to ensure normality of the cohort for dependent
variables. With normality confirmed, two-way repeated measures
ANOVAs (Condition × distance) were used to analyze changes
in RPE, FS and pain. One-way repeated measures ANOVAs
were used to analyze changes in total duration and average
power, as well as 1-km duration and mean power. Two-way
repeated measures ANOVAs (Condition × time) were used to
analyze changes between BASE, PRE, and POST measurements
for MVC, evoked response to magnetic stimulation and PPT.
Percentage change between measurements (BASE-PRE and PREPOST) was also investigated. To investigate pacing profiles,
mean power and RMSsum were analyzed over 250-m using
repeated measures ANOVAs (Condition × distance). Given
inter-participant differences in TTs, power output is expressed
as a product of an individual’s mass (W/kg). When sphericity
Frontiers in Physiology | www.frontiersin.org
Pacing
There was no interaction (Condition × distance) effect for mean
power over 250-m intervals [F (38, 456) = 0.77, P = 0.83, η2p
= 0.06]. All TTs exhibited a similar pacing strategy, however
there was greater variability in mean power in the first 750-m
(Figure 4A). To investigate the variability at the start of the TTs,
one-way repeated measures ANOVAs between distance points
were conducted at 250-m [F (1.78, 21.36) = 0.55 P = 0.56, η2p =
0.04], 500-m [F (1.66, 19.91) = 1.39 P = 0.27 η2p = 0.10] and 750m [F (1.69, 20.33) = 1.31 P = 0.29, η2p = 0.10]. Moderate effects
5
February 2017 | Volume 8 | Article 26
Hibbert et al.
TENS and Exercise
TABLE 2 | Subjective ratings for exertion, affect and pain at each kilometer of TTs.
1- km
2-km
3-km
4-km
5-km
Trial effect
Distance effect
Interaction
CONT
11.69 ± 1.44
12.85 ± 1.77
13.69 ± 1.93
14.88 ± 2.38
16.77 ± 1.96
P = 0.12 η2p = 0.16
P < 0.01 η2p = 0.82
P = 0.58 η2p = 0.16
PLAC
11.85 ± 1.68
13.00 ± 1.41
14.31 ± 1.25
15.00 ± 1.58
17.31 ± 1.75
TENS
12.23 ± 0.73
13.62 ± 1.12
14.54 ± 1.27
15.31 ± 1.65
17.15 ± 1.52
CONT
1.69 ± 1.88
0.54 ± 1.71
−0.23 ± 1.92
−0.54 ± 2.15
−1.31 ± 2.46
P = 0.72 η2p = 0.03
P < 0.01 η2p = 0.69
P = 0.68 η2p = 0.06
PLAC
1.15 ± 1.41
0.46 ± 1.56
−0.31 ± 1.84
−0.62 ± 2.14
−0.92 ± 2.84
TENS
1.15 ± 1.57
0.38 ± 1.66
−0.31 ± 1.84
−0.85 ± 2.30
−1.31 ± 2.66
CONT
2.19 ± 1.79
2.96 ± 2.09
3.92 ± 2.29
4.62 ± 2.73
6.12 ± 2.87
P = 0.68 η2p = 0.03
P < 0.01 η2p = 0.73
P = 0.68 η2p = 0.05
PLAC
1.92 ± 1.31
2.92 ± 1.71
3.58 ± 1.89
4.38 ± 2.36
5.77 ± 2.62
TENS
2.50 ± 2.21
2.81 ± 1.44
3.54 ± 1.90
4.35 ± 2.10
6.08 ± 2.36
RPE
FS
PAIN
Data presented as mean ± SD. RPE, Rate of perceived exertion; FS, feeling scale; Pain, perceived quadriceps pain; CONT, control. PLAC, placebo. TENS, TENS condition. ηp2 , partial
eta squared. Significant distance effects are not shown.
TABLE 3 | Raw changes in PPT, MVC, CAR, and Qtw,pot.
BASE
PRE
POST
Trial effect
Time effect
Interaction
5.23 ± 3.93
4.99 ± 3.57
5.35 ± 3.42
P = 0.47 η2p = 0.07
P = 0.10 η2p = 0.19
P = 0.90 η2p = 0.02
P = 0.97 η2p < 0.01
P < 0.01 η2p = 0.68
P < 0.05 η2p = 0.18
P = 0.70 η2p = 0.04
P = 0.81 η2p = 0.02
P = 0.44 η2p = 0.10
P = 0.10 η2p = 0.17
P < 0.01 η2p = 0.80
P = 0.22 η2p = 0.11
PPT (KGF)
CONT
PLAC
4.76 ± 3.28
4.53 ± 2.60
5.35 ± 4.30
TENS
5.17 ± 2.32
5.12 ± 2.80
5.63 ± 3.82
MVC (N)
CONT
262.70 ± 78.04
254.19 ± 72.33
207.90 ± 63.19*
PLAC
259.52 ± 84.58
251.71 ± 66.23
211.54 ± 66.23*
TENS
271.16 ± 68.04
251.73 ± 74.32#
197.55 ± 61.96*
CAR
CONT
95.26 ± 3.16
95.18 ± 2.65
94.66 ± 4.36
PLAC
94.41 ± 3.48
94.89 ± 2.25
95.46 ± 2.41
TENS
96.72 ± 3.42
95.17 ± 2.93
95.19 ± 2.31
28.76 ± 8.75
26.93 ± 8.45
14.23 ± 7.15*
QTW,POT (N)
CONT
PLAC
28.10 ± 7.84
27.44 ± 8.04
15.39 ± 8.44*
TENS
30.34 ± 10.09
28.38 ± 9.82#
16.34 ± 9.87*
Data presented as mean ± SD. BASE, baseline; PRE, pre-exercise; POST, post-exercise; PPT, pressure pain threshold; MVC, maximal voluntary contraction; CAR, Quadriceps central
activation ratio, for CAR n = 10. Qtw,pot, potentiated quadriceps twitch. CONT, control; PLAC, placebo; TENS, TENS condition; ηp2 , partial eta squared; Time point effects * difference
to BASE and PRE measurement, # difference to BASE measurement.
Post-hoc tests for M-wave amplitude time effects revealed no difference between means.
sizes were observed at 500-m and 750-m. EMG data followed a
similar pattern to power output with no significant interaction
(Condition × distance) effect [F (40, 480) = 1.01, P = 0.46, η2p =
0.08] (Figure 4B). Furthermore, greater variability between TTs
was shown with large effects at 250-m [F (1.5, 18.3) = 2.31, P =
0.14, η2p = 0.16], 500-m [F (1.7, 20.3) = 2.05, P = 0.16, η2p = 0.15]
and 750-m [F (1.6, 18.8) = 2.01, P = 0.17, η2p = 0.14].
and PRE measurements. This difference was not apparent when
expressed as a percentage change from BASE-PRE measurements
(see Table 4). Rather, MVC revealed a main effect of time
with an exercise-induced reduction in all conditions, but no
significant interaction (Condition × time). Mean Qtw,pot
followed MVC values with all conditions having an exerciseinduced reduction PRE-POST (see Tables 3, 5). Only TENS
condition had a reduction in raw Qtw,pot between BASE and
PRE measurements, but a non-significant percentage change
(BASE-PRE) (see Table 5). There was no reduction in quadriceps
CAR as a raw value (see Table 3) or as a percentage change (see
Table 4). Percentage change responses to magnetic stimulation
Fatigue Measurements
An exercise-induced reduction in MVC was recorded PRE
to POST in all conditions (see Table 3), with only TENS
application resulting in a significant reduction between BASE
Frontiers in Physiology | www.frontiersin.org
6
February 2017 | Volume 8 | Article 26
Hibbert et al.
TENS and Exercise
TABLE 4 | Percentage changes in PPT, MVC and CAR.
BASE—PRE Exercise
PRE Exercise—POST Exercise
Trial effect
Time effect
Interaction
P = 0.98 η2p < 0.01
P = 0.08 η2p = 0.25
P = 0.99 η2p < 0.01
P = 0.04 η2p = 0.24
P < 0.01 η2p = 0.66
P = 0.76 η2p = 0.02
P = 0.38 η2p = 0.10
P = 0.65 η2p = 0.02
P = 0.50 η2p = 0.07
PPT (KGF)
CONT
−2.67 ± 19.07
6.65 ± 33.34
PLAC
−1.71 ± 10.18
6.81 ± 22.49
TENS
−2.56 ± 16.34
5.59 ± 22.37
MVC (N)
CONT
−2.51 ± 4.95
−17.46 ± 10.35*
PLAC
−2.18 ± 7.05
−14.75 ± 12.89*
TENS
−8.27 ± 8.92
−20.60 ± 13.74*
−0.06 ± 1.81
−0.54 ± 3.90
PLAC
0.59 ± 3.13
0.65 ± 3.34
TENS
−1.54 ± 3.20
0.07 ± 2.53
CAR
CONT
Data presented as mean percentage change between measurements ± SD. BASE, baseline; PRE, pre-exercise; POST, post-exercise; PPT, pressure pain threshold; MVC, maximal
voluntary contraction; CAR, Quadriceps central activation ratio, for CAR n = 10. CONT, control; PLAC, placebo; TENS, TENS condition. ηp2 , partial eta squared; Time point effects *
difference to BASE—PRE. Post-hoc tests for MVC trial effect revealed no significant difference.
power indicate a possible difference in favor of TENS compared
with PLAC. At the start of trials, moderate to large effect sizes
indicate differences in power output and EMG data. This suggests
a possible influence of TENS on anticipation and, consequently,
the selection of an initial exercise intensity.
Pacing and Performance
The application of TENS was associated with a large effect on
EMG and a moderate effect on power output at the start of
the TT, suggesting that TENS application may have influenced
participant’s anticipation of the task (see Figures 2–4). Afferent
feedback is important in setting an initial exercise intensity
(Tucker, 2009). This is evident with reduced starting exercise
intensities when homeostasis is threatened (Amann et al.,
2007; Schlader et al., 2011). Consequently, exercise intensity
is reduced in order to limit excessive levels of fatigue and
maintain homeostasis. Our results seem to indicate that TENS
application possibly limits afferent feedback activity prior to
exercise, resulting in greater muscle recruitment (as inferred
from EMG data) and power output at the start of the TT. This
supports research indicating a higher intensity is chosen when
afferent information is removed or modified (Amann et al.,
2009). It is likely that this occurs due to the lack of feedback
to inform on potential or actual muscle damage and metabolic
activity. This would indicate to the brain that more work can
be done without indication of serious consequences, creating a
greater neural drive to exercising muscle.
TENS is shown to influence motor neuron excitability
(Hopkins et al., 2002; Pietrosimone et al., 2009). In this
perspective, it is interesting to note that TENS increased EMG
activity, a surrogate for muscle recruitment (Ansley et al., 2004),
at the start of the TT. This enhanced central neural drive was
concomitant to a higher power output. Importantly, TENS did
not produce any change in M-wave responses from BASE to
PRE, indicating no change in resting muscle function before the
cycling TT (see Table 5). However, another possible explanation
FIGURE 1 | Mean ± SD TENS belief ratings. Participants ratings of pain
relief (Pain) and subsequent influence on performance (Performance). PLAC,
placebo; TENS, TENS condition. Ratings are expressed on a 1–10 scale (1; a
bit, 10; a lot). * indicates a difference for pain, P < 0.05. ** indicates a
difference for performance P < 0.01.
are shown in Table 5. There was an exercise-induced reduction
in all measures, except M-wave variables.
DISCUSSION
This is the first study to investigate the influence of TENS
administered prior to a 5-km TT, on exercise-induced pain,
with a focus on influencing exercise intensity and increasing
performance. It was hypothesized, TENS application would
adjust the threshold for sensing pain, allowing for increased
power output for the same rating of pain. As hypothesized, TENS
failed to significantly influence within-exercise subjective pain
ratings, but no significant effect on pacing and performance was
observed. However, a large effect size for TT duration and mean
Frontiers in Physiology | www.frontiersin.org
7
February 2017 | Volume 8 | Article 26
Hibbert et al.
TENS and Exercise
FIGURE 2 | Mean ± SD TT performance measures. TT mean power output (W/kg) (A), 1-km mean power output (W/kg) (B), TT duration (s) (C), and 1-km
duration (s) (D). CONT, control; PLAC, placebo; TENS, TENS condition.
FIGURE 3 | Individual changes for TT performance measures. TT mean power output (W/kg) (A), 1-km mean power output (W/kg) (B), TT duration (s) (C), and
1-km duration (s) (D). CONT, control; PLAC, placebo; TENS, TENS condition.
stimulation which may require a greater neural drive to be
produced. Alternatively, there is an association between TENS
and greater local blood flow (Hallen et al., 2010). This may lead
to a greater activation of type I muscle fibers which are related
to cycling efficiency, thus increasing EMG activity (Coyle et al.,
1992). These possible factors may explain the observed increase
for this result is that neuromuscular electrical stimulation can
change voluntary muscle recruitment patterns, allowing for nonsequential activation of muscle fibers (Gregory and Bickel, 2005).
Yet, stimulation protocols showing these effects are different
to the method utilized in this study. It is possible this effect
occurred, creating a poor recruitment of muscle after TENS
Frontiers in Physiology | www.frontiersin.org
8
February 2017 | Volume 8 | Article 26
Hibbert et al.
TENS and Exercise
FIGURE 4 | TT pacing measures. Group mean power output (A) and electromyography (RMSsum) profiles (B). Mean power output is averaged over 250-m
intervals. RMSsum data is reported as a percentage of a pre-exercise sprint value, RMSsum was measured for 20-s at 250-m intervals. Error bars have been
excluded for clarity. CONT, control; PLAC, placebo; TENS, TENS condition.
in EMG readings, allowing for higher muscle recruitment and
greater power output during the early part of the TENS condition
TT. However, we cannot identify the primary source from this
investigation.
After the initial differences, all TTs exhibit a similar power
output and EMG readings beyond one kilometer (Figure 4). An
initial aggressive pacing strategy would likely assist performance
in shorter tasks such as a 5-km TT (Abbiss and Laursen, 2008).
This would create greater mechanical and chemical stimuli likely
to trigger conscious awareness and influence pain perceptions
(Swart et al., 2012; Edwards and Polman, 2013; Mauger, 2014). It
is possible that this occurred in our study at approximately one
kilometer, with increased exercise-induced stimuli diminishing
the effectiveness of TENS. This may indicate that afferent
information from active skeletal muscles is now unaffected and
the participant uses this to pace performance. It is also likely
at this stage of the intense exercise, feedback from a number
of different sources, not just the active muscle, is pushing the
individual close to their tolerance limit (Hureau et al., 2016).
For these reasons, even with the non-significant differences in
intensity at the start of the trial, it is not surprising observe
similar subjective responses for pain, feeling and exertion in
all conditions. Therefore, these results support the theory that
exercise is regulated in part by afferent feedback to a perceived
Frontiers in Physiology | www.frontiersin.org
pain threshold (Mauger et al., 2010), which presumably plays a
role in a global sensory tolerance limit (Hureau et al., 2016).
Practical Implications
Application of TENS did not provide any overall performance
improvement for a 5-km TT. However, there was a large effect
size for TT duration and moderate effect size for duration
of the first kilometer (see Figures 2, 3). These results provide
some support for the potential of TENS to increase exercise
performance. Participants completed the first kilometer of the
TTs within a range of 95.44–136.28-s, and the difference
between TENS and CONT conditions being −3.12 ± 5.58-s.
Therefore, this research identifies that any possible benefit
of TENS administered prior to exercise may be limited to
events of ≤2 min and where exercise-induced pain is localized.
However, the possible reduction in pain to increase exercise
intensity poses ethical concerns for athlete safety. Administering
an analgesic intervention will augment stimuli that warns of
potential muscle damage, this creates the potential for a greater
risk of injury through increased exercise intensity. Our study
found no significant impact on exercise intensity, but also no
indication of greater exercise-induced fatigue due to TENS
application (i.e., PRE-POST measurement, see Tables 3–5). It
may be of benefit for future investigations to confirm if effects
9
February 2017 | Volume 8 | Article 26
Hibbert et al.
TENS and Exercise
TABLE 5 | Percentage changes in evoked responses to magnetic stimulation.
BASE—PRE Exercise
PRE Exercise—POST Exercise
Trial effect
Time effect
Interaction
P = 0.48 η2p = 0.06
P < 0.01 η2p = 0.83
P = 0.38 η2p = 0.08
P = 0.48 η2p = 0.06
P < 0.01 η2p = 0.86
P = 0.24 η2p = 0.11
P = 0.44 η2p = 0.07
P < 0.01 η2p = 0.65
P = 0.33 η2p = 0.09
P = 0.22 η2p = 0.12
P < 0.01 η2p = 0.88
P = 0.78 η2p = 0.01
P = 0.19 η2p = 0.13
P < 0.01 η2p = 0.56
P = 0.12 η2p = 0.16
P = 0.22 η2p = 0.12
P = 0.07 η2p = 0.26
P = 0.45 η2p = 0.06
P = 0.17 η2p = 0.14
P = 0.49 η2p = 0.04
P = 0.25 η2p = 0.11
QTW,POT (N)
CONT
−5.09 ± 13.11
−46.75 ± 17.59*
PLAC
−2.25 ± 8.02
−44.56 ± 20.52*
TENS
−5.92 ± 9.11
−41.43 ± 26.33*
CONT
−3.91 ± 11.92
−56.73 ± 19.73*
PLAC
−2.62 ± 9.31
−54.14 ± 20.78*
TENS
−3.35 ± 16.81
−48.54 ± 23.32*
CONT
−0.61 ± 12.50
−23.78 ± 13.92*
PLAC
−1.77 ± 18.50
−20.24 ± 12.60*
TENS
4.74 ± 12.30
−23.87 ± 11.37*
MRFD (N.S−1 )
CT (S)
MRR (N.S−1 )
CONT
−6.03 ± 19.81
−59.36 ± 15.22*
PLAC
−2.70 ± 23.36
−53.31 ± 22.34*
TENS
−0.40 ± 10.04
−55.59 ± 23.30*
CONT
−5.09 ± 13.25
−23.32 ± 19.02*
PLAC
−3.15 ± 23.57
−21.98 ± 18.74*
TENS
7.09 ± 17.06
−26.85 ± 15.85*
RT0.5 (N.S−1 )
M-WAVE AMPLITUDE (MV)
CONT
PLAC
TENS
2.63 ± 18.83
−0.66 ± 7.73
1.89 ± 16.14
4.75 ± 13.50
3.03 ± 10.91
13.85 ± 21.50
M-WAVE DURATION (MS)
CONT
−4.71 ± 14.21
−7.11 ± 24.17
PLAC
1.07 ± 17.25
7.96 ± 16.49
TENS
−9.07 ± 37.90
−7.05 ± 27.86
Data presented as mean percentage change between measurements ± SD. BASE, baseline; PRE, pre-exercise; POST, post-exercise; Qtw,pot, potentiated quadriceps twitch; MRFD,
maximal rate of force development; CT, contraction time; MRR, maximal rate of relaxation; RT0.5 , one-half relaxation time; CONT, control; PLAC, placebo; TENS, TENS condition; ηp2 ,
partial eta squared. Time point effects * difference to BASE—PRE.
there may be merit in use of TENS as a within-exercise training
intervention (Hughes et al., 2013).
of TENS application occur in elite populations, to highlight any
potential benefits or concerns of TENS use.
One possible future investigation could look at potential
benefits of TENS use within a task. We tested the use of TENS
prior a task, with a 5-km TT chosen in anticipation that exercise
would be conducted in a proposed post-stimulation analgesic
period. Compared to a longer task (e.g., 20-km TT), a greater
exercise intensity would be observed in a 5-km TT, and therefore,
a greater nociceptive stimulus is expected. Accordingly, when
pain is greater, it may be harder to distinguish small changes
in pain perceptions that an intervention may provide. Also
theoretically, it is possible that TENS could be beneficial for
longer duration tasks which are more reliant on afferent feedback
for regulation (Tucker, 2009; Mauger et al., 2010), and where
pain perceptions are expected to be less prominent. Furthermore,
TENS is more likely to reduce pain perceptions when stimulation
is active. Therefore, future investigations into the possible use
of TENS to enhance exercise performance may look at utilizing
TENS during trials of greater length. Ethically, it is unlikely TENS
could be used within a sporting event due to doping concerns, but
Frontiers in Physiology | www.frontiersin.org
Limitations
There are several limitations in this study. Perceptions of TENS
for pain relief and influence on performance were greater
than PLAC condition (see Figure 1). Measures were taken to
minimize the influence of any placebo effect of TENS. However,
participants would have clearly felt a difference in sensation
between TENS and PLAC conditions. Furthermore, participants
were made aware of the aims of the study, and informed they
were receiving high or low TENS, but not aware of which
intervention was placebo. This could have had implications on
the results shown by TENS (Son et al., 2016). Placebo effects have
been shown to influence exercise pain perceptions (Benedetti
et al., 2007) but also the ability to produce force (Broatch et al.,
2014). As participant’s perceptions of TENS effectiveness on pain
relief and performance were increased post study compared to
PLAC condition (Figure 1), this could have produced changes at
the start of the 5-km TT.
10
February 2017 | Volume 8 | Article 26
Hibbert et al.
TENS and Exercise
gate control of pain and reduce feedback from group III and IV
afferents (Moran et al., 2011). However, amplitude, stimulation
duration, prior use and tolerance of opioids can compromise
TENS effectiveness (Sluka et al., 2013). Participants currently
taking pain medication were excluded from the study, but the
prior use of opioids was not recorded. Typically, peak effects for
analgesia provided by TENS will be greater when stimulation
is active, or immediately after cessation (Moran et al., 2011;
Vance et al., 2012). For this research, we conducted a 5-km
TT, as we anticipated post-stimulation effects for approximately
30-min would be present (Moran et al., 2011). As expected,
within-exercise pain perceptions were similar, but there is an
absence of significant differences in exercise intensity. Therefore,
by administering the intervention prior to exercise, it is possible
that analgesic effectiveness of TENS for this mode of exercise is
reduced.
Although the current study has several limitations, the overall
multidisciplinary approach allows for assessment of a number of
variables related to exercise performance. The aim of the study
was to assess the efficacy of TENS on exercise performance,
with a focus on exercise-induced pain. Although there were no
significant differences in pain and performance, the reporting of
multiple variables related to exercise intensity, fatigue but also
psychological aspects represent strengths of this study.
With physiological differences between participants, it is
possible that there are responders and non-responders to this
type of intervention (Figure 3). For example, the amount
of subcutaneous fat may affect the amplitude of stimulation
to afferent fibers (Hughes et al., 2013). Hence, those with
lower body fat may not be able to increase the amplitude of
stimulation to a level that will stimulate deeper tissue (Hughes
et al., 2013). This could possibly result in different levels of
stimulation between participants, leading to differing levels of
afferent information, and effect on performance. This is a
limitation of the study, as the final current intensity was not
recorded, we cannot confirm the dose received by participants.
However, application of TENS was adjusted to an individual’s
own sensory threshold, in effect an individual’s tolerance of the
stimulation. It has to be noted that applying a TENS intensity
higher than what a participant can tolerate would be unethical.
However, it could be speculated that those who responded to
the intervention (i.e., higher initial power output) (Figures 2,
3) were able to tolerate a higher current intensity during TENS
application.
The potential of TENS to affect exercise-induced pain
was based on previous research in pain-free individuals that
influenced PPT (Moran et al., 2011), but also restored muscle
strength when pain was induced (Son et al., 2016). Recent
research however, has indicated a possibility for different
subgroups of group III and IV muscle afferents which are
sensitive to distinct metabolites. One subgroup is likely to
respond to intramuscular metabolites associated with aerobic
exercise, whilst another responds to noxious levels of metabolites
(e.g., hypertonic saline) associated with ischemic contractions
(Amann et al., 2015). These differing characteristics of muscle
afferents may be a possible reason why TENS failed to
significantly change exercise intensity within this study. Whilst
in comparison, analgesic effects are demonstrated during exercise
when pain is induced (Son et al., 2016).
Reductions in MVC and Qtw,pot were observed from BASE to
PRE for TENS condition (see Table 3; Moran et al., 2011; Amann
et al., 2015; Son et al., 2016), although percentage reductions were
not significantly different (see Tables 3, 4). This likely resulted
from the stimulation intensity being close to the threshold for
muscle contraction. However, despite this apparent fatigue, it
dissipated quickly as power was greatest in TENS condition early
in the TT (see Figure 4A). Therefore, a possible limitation of
prior to exercise use of TENS may be the application settings.
Application duration should be limited and higher intensities
avoided as this may induce peripheral fatigue that is detrimental
to performance. Furthermore, PRE assessment was conducted
after the cycling warm-up, which may have contributed to the
reduced voluntary force, thus disguising the true influence of
TENS on muscle strength properties. Settings for TENS were
based on previous research indicating this would activate the
Conclusions
In conclusion, this study found no significant effects of TENS
administered prior to exercise on 5-km TT performance,
although similar pain perceptions were observed. This casts
doubt on the effectiveness of the application of TENS prior to
exercise to modify afferent feedback and influence perceptions
of exercise-induced pain. However, there are indications TENS
application may influence neural drive and power output at
the start of a 5-km TT. Aside from any potential changes
in pain perceptions, other possible reasons for this include
psychological belief in the intervention and altered muscle
recruitment. Future research could investigate the effectiveness
of TENS on modifying the sensation of exercise-induced muscle
pain, with a focus on application during other forms of aerobic
exercise.
AUTHOR CONTRIBUTIONS
All authors contributed to the study design. AH collected data,
with AH, FB and RP conducted the initial data analysis. First draft
of manuscript was written by AH, with all authors reviewing the
manuscript and approving the final version.
ACKNOWLEDGMENTS
The authors would like to thank R. Stokes for technical assistance.
REFERENCES
Amann, M., Proctor, L. T., Sebranek, J. J., Pegelow, D. F., and
Dempsey, J. A. (2009). Opioid-mediated muscle afferents inhibit
central motor drive and limit peripheral muscle fatigue development
in humans. J. Physiol. 587, 271–283. doi: 10.1113/jphysiol.2008.
163303
Abbiss, C. R., and Laursen, P. B. (2008). Describing and understanding
pacing strategies during athletic competition. Sports Med. 38, 239–252.
doi: 10.2165/00007256-200838030-00004
Frontiers in Physiology | www.frontiersin.org
11
February 2017 | Volume 8 | Article 26
Hibbert et al.
TENS and Exercise
Hughes, N., Bennett, M. I., and Johnson, M. I. (2013). An investigation into
the magnitude of the current window and perception of transcutaneous
electrical nerve stimulation (TENS) sensation at various frequencies and
body sites in healthy human participants. Clin. J. Pain 29, 146–153.
doi: 10.1097/AJP.0b013e3182579919
Hureau, T. J., Romer, L. M., and Amann, M. (2016). The ‘sensory tolerance limit’:
a hypothetical construct determining exercise performance? Eur. J. Sport Sci.
doi: 10.1080/17461391.2016.1252428. [Epub ahead of print].
Johnson, M. I., Paley, C. A., Howe, T. E., and Sluka, K. A. (2015). Transcutaneous
electrical nerve stimulation for acute pain. Cochrane Database Syst. Rev.
6:CD006142. doi: 10.1002/14651858.CD006142.pub3
Johnson, M., and Martinson, M. (2007). Efficacy of electrical nerve stimulation for
chronic musculoskeletal pain: a meta-analysis of randomized controlled trials.
Pain 130, 157–165. doi: 10.1016/j.pain.2007.02.007
Katayama, K., Sato, K., Matsuo, H., Ishida, K., Iwasaki, K., and Miyamura,
M. (2004). Effect of intermittent hypoxia on oxygen uptake during
submaximal exercise in endurance athletes. Eur. J. Appl. Physiol. 92, 75–83.
doi: 10.1007/s00421-004-1054-0
Kennedy, D. S., McNeil, C. J., Gandevia, S. C., and Taylor, J. L. (2014).
Fatigue-related firing of distal muscle nociceptors reduces voluntary activation
of proximal muscles of the same limb. J. Appl. Physiol. 116, 385–394.
doi: 10.1152/japplphysiol.01166.2013
Kent-Braun, J. A. (1999). Central and peripheral contributions to muscle fatigue in
humans during sustained maximal effort. Eur. J. Appl. Physiol. Occup. Physiol.
80, 57–63. doi: 10.1007/s004210050558
Loeser, J. D., and Treede, R. D. (2008). The kyoto protocol of IASP basic pain
terminology. Pain 137, 473–477. doi: 10.1016/j.pain.2008.04.025
Marshall, P. W. M., Lovell, R., Jeppesen, G. K., Andersen, K., and Siegler, J. C.
(2014). Hamstring muscle fatigue and central motor output during a simulated
soccer match. PLoS ONE 9:e102753. doi: 10.1371/journal.pone.0102753
Mauger, A. R. (2013). Fatigue is a pain-the use of novel neurophysiological
techniques to understand the fatigue-pain relationship. Front. Physiol. 4:104.
doi: 10.3389/fphys.2013.00104
Mauger, A. R. (2014). Factors affecting the regulation of pacing:
current perspectives. Open Access J. Sports Med. 5, 209–214.
doi: 10.2147/OAJSM.S38599
Mauger, A. R., Jones, A. M., and Williams, C. A. (2010). Influence of
acetaminophen on performance during time trial cycling. J. Appl. Physiol. 108,
98–104. doi: 10.1152/japplphysiol.00761.2009
Melzack, R., and Wall, P. D. (1965). Pain mechanisms: a new theory. Science 150,
971–979.
Moran, F., Leonard, T., Hawthorne, S., Hughes, C. M., McCrum-Gardner, E.,
Johnson, M. I., et al. (2011). Hypoalgesia in response to transcutaneous
electrical nerve stimulation (TENS) depends on stimulation intensity. J. Pain
12, 929–935. doi: 10.1016/j.jpain.2011.02.352
O’Bryan, S. J., Brown, N. A., Billaut, F., and Rouffet, D. M. (2014). Changes in
muscle coordination and power output during sprint cycling. Neurosci. Lett.
576, 11–16. doi: 10.1016/j.neulet.2014.05.023
O’Connor, P. J., and Cook, D. B. (1999). Exercise and pain: the neurobiology,
measurement, and laboratory study of pain in relation to exercise in humans.
Exerc. Sport Sci. Rev. 27, 119–166.
O’Connor, P. J., and Cook, D. B. (2001). Moderate-intensity muscle pain can be
produced and sustained during cycle ergometry. Med. Sci. Sports Exerc. 33,
1046–1051. doi: 10.1097/00005768-200106000-00026
Pantaleão, M. A., Laurino, M. F., Gallego, N. L. G., Cabral, C. M. N., Rakel,
B., Vance, C., et al. (2011). Adjusting pulse amplitude during transcutaneous
electrical nerve stimulation (TENS) application produces greater hypoalgesia.
J. Pain 12, 581–590. doi: 10.1016/j.jpain.2010.11.001
Pietrosimone, B. G., Hart, J. M., Saliba, S. A., Hertel, J., and Ingersoll, C. D. (2009).
Immediate effects of transcutaneous electrical nerve stimulation and focal knee
joint cooling on quadriceps activation. Med. Sci. Sports Exerc. 41, 1175–1181.
doi: 10.1249/MSS.0b013e3181982557
Schlader, Z. J., Simmons, S. E., Stannard, S. R., and Mündel, T. (2011). Skin
temperature as a thermal controller of exercise intensity. Eur. J. Appl. Physiol.
111, 1631–1639. doi: 10.1007/s00421-010-1791-1
Sluka, K. A., Bjordal, J. M., Marchand, S., and Rakel, B. A. (2013). What
makes transcutaneous electrical nerve stimulation work? Making sense of
Amann, M., Romer, L. M., Subudhi, A. W., Pegelow, D. F., and Dempsey, J. A.
(2007). Severity of arterial hypoxaemia affects the relative contributions of
peripheral muscle fatigue to exercise performance in healthy humans. J. Physiol.
581, 389–403. doi: 10.1113/jphysiol.2007.129700
Amann, M., Sidhu, S. K., Weavil, J. C., Mangum, T. S., and Venturelli, M. (2015).
Autonomic responses to exercise: group III/IV muscle afferents and fatigue.
Auton. Neurosci. 188, 19–23. doi: 10.1016/j.autneu.2014.10.018
Amann, M., Venturelli, M., Ives, S. J., McDaniel, J., Layec, G., Rossman, M.
J., et al. (2013). Peripheral fatigue limits endurance exercise via a sensory
feedback-mediated reduction in spinal motoneuronal output. J. Appl. Physiol.
115, 355–364. doi: 10.1152/japplphysiol.00049.2013
Ansley, L., Schabort, E., St Clair Gibson, A., Lambert, M. I., and Noakes, T. D.
(2004). Regulation of pacing strategies during successive 4-km time trials. Med.
Sci. Sports Exerc. 36, 1819–1825. doi: 10.1249/01.MSS.0000142409.70181.9D
Benedetti, F., Pollo, A., and Colloca, L. (2007). Opioid-mediated
placebo responses boost pain endurance and physical performance:
is it doping in sport competitions? J. Neurosci. 27, 11934–11939.
doi: 10.1523/JNEUROSCI.3330-07.2007
Billaut, F., Davis, J. M., Smith, K. J., Marino, F. E., and Noakes, T. D.
(2010). Cerebral oxygenation decreases but does not impair performance
during self-paced, strenuous exercise. Acta Physiol. 198, 477–486.
doi: 10.1111/j.1748-1716.2009.02058.x
Billaut, F., Kerris, J. P., Rodriguez, R. F., Martin, D. T., Gore, C. J., and Bishop,
D. J. (2013). Interaction of central and peripheral factors during repeated
sprints at different levels of arterial O2 saturation. PLoS ONE 8:e77297.
doi: 10.1371/journal.pone.0077297
Borg, G. A. (1970). Perceived exertion as an indicator of somatic stress. Scand. J.
Rehabil. Med. 2, 92–98.
Broatch, J. R., Petersen, A., and Bishop, D. J. (2014). Postexercise cold water
immersion benefits are not greater than the placebo effect. Med. Sci. Sports
Exerc. 46, 2139–2147. doi: 10.1249/MSS.0000000000000348
Cheing, G. L. Y., Hui-Chan, C. W. Y., and Chan, K. M. (2002). Does four weeks of
TENS and/or isometric exercise produce cumulative reduction of osteoarthritic
knee pain? Clin. Rehabil. 16, 749–760. doi: 10.1191/0269215502cr549oa
Chen, C. C., and Johnson, M. I. (2010). An investigation into the hypoalgesic effects
of high- and low-frequency transcutaneous electrical nerve stimulation (TENS)
on experimentally-induced blunt pressure pain in healthy human participants.
J. Pain 11, 53–61. doi: 10.1016/j.jpain.2009.05.008
Cohen, J. (1988). Statistical Power Analysis for the Behavioral Sciences, 2nd Edn.
Hillsdale, NJ: Laurence Erlbaum Associates.
Coyle, E. F., Sidossis, L. S., Horowitz, J. F., and Beltz, J. D. (1992). Cycling efficiency
is related to the percentage of Type I muscle fibers. Med. Sci. Sports Exerc. 24,
782–788. doi: 10.1249/00005768-199207000-00008
Dannecker, E. A., Liu, Y., Rector, R. S., Thomas, T. R., Fillingim, R. B.,
and Robinson, M. E. (2012). Sex differences in exercise-induced muscle
pain and muscle damage. J. Pain 13, 1242–1249. doi: 10.1016/j.jpain.2012.
09.014
Edwards, A. M., and Polman, R. C. J. (2013). Pacing and awareness:
brain regulation of physical activity. Sports Med. 43, 1057–1064.
doi: 10.1007/s40279-013-0091-4
Foster, J., Taylor, L., Chrismas, B. C., Watkins, S. L., and Mauger, A. R. (2014).
The influence of acetaminophen on repeated sprint cycling performance. Eur.
J. Appl. Physiol. 114, 41–48. doi: 10.1007/s00421-013-2746-0
Gandevia, S. C. (2001). Spinal and supraspinal factors in human muscle fatigue.
Physiol. Rev. 81, 1725–1789.
Gregory, C. M., and Bickel, C. S. (2005). Recruitment patterns in human skeletal
muscle during electrical stimulation. Phys. Ther. 85, 358–364.
Hallen, K., Hrafnkelsdottir, T., Jern, S., Biber, B., Mannheimer, C., and DuttaRoy,
S. (2010). Transcutaneous electrical nerve stimulation induces vasodilation in
healthy controls but not in refractory angina patients. J. Pain Symptom Manage.
40, 95–101. doi: 10.1016/j.jpainsymman.2009.12.009
Hardy, C. J., and Rejeski, W. J. (1989). Not what, but how one feels: the
measurement of affect during exercise. J. Sport Exerc. Psychol. 11, 304–317.
Hopkins, J. T., Ingersoll, C. D., Edwards, J., and Klootwyk, T. E. (2002).
Cryotherapy and transcutaneous electric neuromuscular stimulation decrease
arthrogenic muscle inhibition of the vastus medialis after knee joint effusion. J.
Athl. Train. 37, 25–31.
Frontiers in Physiology | www.frontiersin.org
12
February 2017 | Volume 8 | Article 26
Hibbert et al.
TENS and Exercise
Ulmer, H. V. (1996). Concept of an extracellular regulation of muscular metabolic
rate during heavy exercise in humans by psychophysiological feedback.
Experientia 52, 416–420.
Vance, C. G., Rakel, B. A., Blodgett, N. P., DeSantana, J. M., Amendola,
A., Zimmerman, M. B., et al. (2012). Effects of transcutaneous electrical
nerve stimulation on pain, pain sensitivity, and function in people with
knee osteoarthritis: a randomized controlled trial. Phys. Ther. 92, 898–910.
doi: 10.2522/ptj.20110183
Vanhatalo, A., Doust, J. H., and Burnley, M. (2007). Determination of critical
power using a 3-min all-out cycling test. Med. Sci. Sports Exerc. 39, 548–555.
doi: 10.1249/mss.0b013e31802dd3e6
Williams, C. A., Bailey, S. D., and Mauger, A. R. (2012). External exercise
information provides no immediate additional performance benefit to
untrained individuals in time trial cycling. Br. J. Sports Med. 46, 49–53.
doi: 10.1136/bjsports-2011-090257
the mixed results in the clinical literature. Phys. Ther. 93, 1397–1402.
doi: 10.2522/ptj.20120281
Smits, B. L. M., Pepping, G. J., and Hettinga, F. J. (2014). Pacing and
decision making in sport and exercise: the roles of perception and
action in the regulation of exercise intensity. Sports Med. 44, 763–775.
doi: 10.1007/s40279-014-0163-0
Son, S. J., Kim, H., Seeley, M. K., Feland, J. B., and Hopkins, J. T. (2016).
Effects of transcutaneous electrical nerve stimulation on quadriceps function
in individuals with experimental knee pain. Scand. J. Med. Sci. Sports 26,
1080–1090. doi: 10.1111/sms.12539
Swart, J., Lindsay, T. R., Lambert, M. I., Brown, J. C., and Noakes, T. D.
(2012). Perceptual cues in the regulation of exercise performance physical sensations of exercise and awareness of effort interact as
separate cues. Br. J. Sports Med. 46, 42–48. doi: 10.1136/bjsports-2011090337
Tofari, P. J., Opar, D. A., Kemp, J. G., Billaut, F., and Cormack, S. (2016). Reliability
of measures of quadriceps muscle function using magnetic stimulation. Muscle
Nerve 53, 770–778. doi: 10.1002/mus.24926
Tomasi, F. P., Chiappa, G., Maldaner da Silva, V., Lucena da Silva, M., Lima,
A. S., Arena, R., et al. (2015). Transcutaneous electrical nerve stimulation
improves exercise tolerance in healthy subjects. Int. J. Sports Med. 36, 661–665.
doi: 10.1055/s-0034-1387763
Tucker, R. (2009). The anticipatory regulation of performance: the physiological
basis for pacing strategies and the development of a perceptionbased model for exercise performance. Br. J. Sports Med. 43, 392–400.
doi: 10.1136/bjsm.2008.050799
Frontiers in Physiology | www.frontiersin.org
Conflict of Interest Statement: The authors declare that the research was
conducted in the absence of any commercial or financial relationships that could
be construed as a potential conflict of interest.
Copyright © 2017 Hibbert, Billaut, Varley and Polman. This is an open-access article
distributed under the terms of the Creative Commons Attribution License (CC BY).
The use, distribution or reproduction in other forums is permitted, provided the
original author(s) or licensor are credited and that the original publication in this
journal is cited, in accordance with accepted academic practice. No use, distribution
or reproduction is permitted which does not comply with these terms.
13
February 2017 | Volume 8 | Article 26