Effects of Neuromuscular Electrical Stimulation Training on Endurance Performance

Abstract

Various electrical stimulation modalities are used as adjuvants to conventional training and rehabilitation programs to increase bodily function or to reduce symptoms, such as pain. One of these modalities, neuromuscular electrical stimulation (NMES), commonly refers to the transcutaneous application of electrical currents to a target muscle group with the objective to depolarize motor neurons and consequently elicit skeletal muscle contractions of substantial intensity (usually ranging from 10 to 60% of the maximal voluntary contraction). Because NMES can generate considerable muscle tension, it is frequently used as a strength training technique for healthy adults and athletes, but also as a rehabilitation tool to increase or preserve muscle function and mass in individuals with muscle weakness or patients who cannot perform voluntary contractions [e.g., patients suffering from chronic heart failure (CHF), chronic obstructive pulmonary disease (COPD), or critical illness; for reviews, see Roig and Reid, 2009; Sillen et al., 2009; Sbruzzi et al., 2010; Maddocks et al., 2011; Maffiuletti et al., 2011; Smart et al., 2013; Burke et al., 2016]. Under certain conditions, NMES training may also improve muscle oxidative capacity and result in a fast-to-slow muscle fiber type transition (Perez et al., 2002; Gondin et al., 2011a), which could potentially enhance endurance performance. However, the relevance of such adaptations in skeletal muscle tissue for the translation to functional performance that is particularly important for sport and daily activities is not always self-evident, mainly because of the heterogeneity in study populations, NMES parameters, and outcome measures. Unfortunately, the bodies of literature that either focus on mechanistic (i.e., muscle endurance) or clinical (i.e., functional endurance) outcomes are often too disconnected. In this opinion paper, we aim to bring these bodies of literature together and discuss the impact of high- vs. low-frequency NMES training on muscle vs. functional endurance in healthy vs. clinical populations. As such, we focus on human studies that chronically applied NMES for at least 3 weeks in healthy persons and patients, and distinguish between the effectiveness of non-tetanic low-frequency NMES (that is usually administered continuously at frequencies close to 10 Hz) and tetanic high-frequency NMES (that is usually administered intermittently at frequencies close to 50 Hz) on muscle endurance and functional endurance. For clarity purposes, we refer to muscle endurance as the exercise-induced decline in voluntary or electrically-evoked force (Duchateau and Hainaut, 1988; Gondin et al., 2006) or the endurance time of a sustained single-joint contraction (Gondin et al., 2006). In contrast, we refer to functional endurance as the maximal oxygen consumption or workload (Perez et al., 2002; Porcelli et al., 2012), the distance covered in a given time (e.g., 6-minute walk test) or the endurance time (Kim et al., 1995) for whole-body exercises such as walking and cycling. In the last section, we will provide some recommendations for better clinical use of NMES, and suggest potential directions for future research.

Full text

OPINION
published: 16 November 2016
doi: 10.3389/fphys.2016.00544
Frontiers in Physiology | www.frontiersin.org 1November 2016 | Volume 7 | Article 544
Edited by:
Benjamin Pageaux,
Université de Bourgogne, France
Reviewed by:
Roger Enoka,
University of Colorado, USA
*Correspondence:
Nicola A. Maffiuletti
nicola.maffiuletti@kws.ch
Specialty section:
This article was submitted to
Exercise Physiology,
a section of the journal
Frontiers in Physiology
Received: 14 October 2016
Accepted: 28 October 2016
Published: 16 November 2016
Citation:
Veldman MP, Gondin J, Place N and
Maffiuletti NA (2016) Effects of
Neuromuscular Electrical Stimulation
Training on Endurance Performance.
Front. Physiol. 7:544.
doi: 10.3389/fphys.2016.00544
Effects of Neuromuscular Electrical
Stimulation Training on Endurance
Performance
Menno P. Veldman 1, 2, Julien Gondin 3, Nicolas Place 4,5 and Nicola A. Maffiuletti 2*
1Center for Human Movement Sciences, University Medical Center, Groningen, Netherlands, 2Human Performance Lab,
Schulthess Clinic, Zurich, Switzerland, 3Institut NeuroMyoGène, Université Claude Bernard Lyon 1, INSERM U1217, CNRS
UMR 5310, Villeurbanne, France, 4Institute of Sport Sciences, University of Lausanne, Lausanne, Switzerland, 5Department
of Physiology, Faculty of Biology and Medicine, University of Lausanne, Lausanne, Switzerland
Keywords: neuromuscular electrical stimulation, skeletal muscle, muscle endurance, functional endurance,
rehabilitation
INTRODUCTION
Various electrical stimulation modalities are used as adjuvants to conventional training and
rehabilitation programs to increase bodily function or to reduce symptoms, such as pain.
One of these modalities, neuromuscular electrical stimulation (NMES), commonly refers to the
transcutaneous application of electrical currents to a target muscle group with the objective
to depolarize motor neurons and consequently elicit skeletal muscle contractions of substantial
intensity (usually ranging from 10 to 60% of the maximal voluntary contraction). Because NMES
can generate considerable muscle tension, it is frequently used as a strength training technique
for healthy adults and athletes, but also as a rehabilitation tool to increase or preserve muscle
function and mass in individuals with muscle weakness or patients who cannot perform voluntary
contractions [e.g., patients suffering from chronic heart failure (CHF), chronic obstructive
pulmonary disease (COPD), or critical illness; for reviews, see Roig and Reid, 2009; Sillen et al.,
2009; Sbruzzi et al., 2010; Maddocks et al., 2011; Maffiuletti et al., 2011; Smart et al., 2013;
Burke et al., 2016]. Under certain conditions, NMES training may also improve muscle oxidative
capacity and result in a fast-to-slow muscle fiber type transition (Pérez et al., 2002; Gondin
et al., 2011a), which could potentially enhance endurance performance. However, the relevance
of such adaptations in skeletal muscle tissue for the translation to functional performance that is
particularly important for sport and daily activities is not always self-evident, mainly because of
the heterogeneity in study populations, NMES parameters, and outcome measures. Unfortunately,
the bodies of literature that either focus on mechanistic (i.e., muscle endurance) or clinical (i.e.,
functional endurance) outcomes are often too disconnected. In this opinion paper, we aim to
bring these bodies of literature together and discuss the impact of high- vs. low-frequency NMES
training on muscle vs. functional endurance in healthy vs. clinical populations. As such, we focus
on human studies that chronically applied NMES for at least 3 weeks in healthy persons and
patients, and distinguish between the effectiveness of non-tetanic low-frequency NMES (that is
usually administered continuously at frequencies close to 10 Hz) and tetanic high-frequency NMES
(that is usually administered intermittently at frequencies close to 50 Hz) on muscle endurance and
functional endurance. For clarity purposes, we refer to muscle endurance as the exercise-induced
decline in voluntary or electrically-evoked force (Duchateau and Hainaut, 1988; Gondin et al., 2006)
or the endurance time of a sustained single-joint contraction (Gondin et al., 2006). In contrast,
we refer to functional endurance as the maximal oxygen consumption or workload (Pérez et al.,
2002; Porcelli et al., 2012), the distance covered in a given time (e.g., 6-minute walk test) or the
endurance time (Kim et al., 1995) for whole-body exercises such as walking and cycling. In the

Veldman et al. Electrical Stimulation and Endurance Performance
last section, we will provide some recommendations for better
clinical use of NMES, and suggest potential directions for future
research.
EFFECTS OF NMES TRAINING ON
ENDURANCE PERFORMANCE IN
HEALTHY SUBJECTS
High-frequency NMES training enhances muscle strength (for
a review, see Gondin et al., 2011b), but may not affect
(Duchateau and Hainaut, 1988) or even decrease muscle
endurance, as demonstrated for example by a reduced ability to
sustain a submaximal contraction (Gondin et al., 2006). High-
frequency NMES training also appears to have a negligible
influence on functional endurance, as illustrated for example
by maximal oxygen consumption results (Figure 1A) (Pérez
et al., 2002; Porcelli et al., 2012). These limited effects of
high-frequency NMES training on endurance performance are
somewhat surprising for different reasons. First, a single session
of high-frequency NMES induces an exaggerated metabolic
and cardiovascular stress when compared to torque-matched
voluntary contractions (McNeil et al., 2006; Theurel et al., 2007)
and high levels of muscle fatigue, mainly due to the motor
unit recruitment pattern of NMES that is considerably different
from voluntary contractions (for a review, see Bickel et al.,
2011). Second, high-frequency NMES results in a fast-to-slow
shift in fiber type distribution together with increased oxidative
capacity and capillarization of the stimulated muscles (Pérez
et al., 2002; Gondin et al., 2011a), i.e., adaptations that are
characteristic of endurance training. However, methodological
limitations pertaining to the definition and assessment of muscle
or functional endurance complicate the interpretation of the data.
Also, the evaluation of endurance for commonly-used muscles
such as the quadriceps in normally functioning people may not
be optimal as it likely suffers from ceiling effects. This suggestion
is confirmed by the observation that high-frequency NMES
training of abdominal muscles in healthy individuals resulted in
substantial increases in abdominal strength and endurance time
(Alon et al., 1987).
Data on the effects of low-frequency NMES training
on muscle and functional endurance in healthy participants
are relatively scarce. Three studies show improvements in
functional endurance following low-frequency NMES training
(e.g., improved work capacity and oxygen consumption at
the anaerobic threshold), possibly mediated by adaptations
in aerobic-oxidative metabolism and increased capillarization
(Thériault et al., 1996; Nuhr et al., 2003; Miyamoto et al.,
2016). Notwithstanding the limited data, the effects of low-
frequency NMES training on functional endurance appear in
general superior to those induced by high-frequency NMES
training, despite the apparently similar fast-to-slow transition
in fiber type distribution induced by the two NMES modalities
(Thériault et al., 1996; Nuhr et al., 2003). Such divergent
effectiveness of high- vs. low-frequency NMES training on
endurance performance is likely caused by methodological
differences between the two modalities. High-frequency NMES is
usually applied intermittently and with higher current intensities
in comparison with low-frequency NMES. Because of better
current tolerance, low-frequency NMES sessions are generally
considerably longer and can reach up to 240 min of continuous
stimulation per day (e.g., Nuhr et al., 2003), vs. 20–30 min
of intermittent high-frequency NMES per day (Gondin et al.,
2011a). Such differences may have contributed to the greater
increases in functional endurance observed after low- vs. high-
frequency NMES training and strongly suggest that the long
duration of low-frequency NMES sessions may be the most
important parameter for increasing functional endurance.
In summary, little is known about the impact of NMES
training on muscle and functional endurance in a healthy
population. High-frequency NMES training has no influence or
may even have a negative impact on muscle endurance while
for functional endurance, low-frequency NMES training appears
favorable, possibly because of the very long treatment sessions.
Studies in healthy individuals that often targeted the quadriceps
muscle may have suffered from ceiling effects. We speculate
that NMES interventions on less-used muscle groups and with
stronger study designs (large sample size, homogeneous subject
characteristics, sham condition) will provide more insights into
the real effectiveness of NMES training.
EFFECTS OF NMES TRAINING ON
ENDURANCE PERFORMANCE IN PATIENT
POPULATIONS
The suggestion that less-used muscle groups are more prone to
improvement is confirmed by findings obtained in patients with
pathologies affecting muscle, pulmonary, and cardiovascular
function. In general, NMES training protocols are more effective
in patients compared to healthy individuals, at least for functional
endurance (Figure 1A). In various patient groups such as
COPD and CHF, NMES training improved muscle strength and
respiratory function, and consequently, functional endurance
as reflected by increased oxygen uptake and workload, longer
endurance times and farther movement distances, often indexed
by the 6-minute walk test (for reviews, see Roig and Reid, 2009;
Sillen et al., 2009; Sbruzzi et al., 2010; Maddocks et al., 2011;
Smart et al., 2013; Burke et al., 2016). In contrast, there are few
data on adaptations in muscle endurance after high- or low-
frequency NMES training in patient populations. To the best
of our knowledge, only three studies reported improvements in
muscle endurance in different patient groups following NMES
interventions (Quittan et al., 2001; Doucet and Griffin, 2013;
Erickson et al., 2016). Clinical trials that applied high- and
low-frequency NMES training focused mostly on functional
endurance because of its clinical relevance (Vaquero et al., 1998;
Bourjeily-Habr et al., 2002; Neder et al., 2002; Harris et al., 2003;
Nuhr et al., 2003; Eicher et al., 2004; Banerjee et al., 2005; Deley
et al., 2005; Dobsák et al., 2006; Karavidas et al., 2006; LeMaitre
et al., 2006; Vivodtzev et al., 2006, 2012; Dal Corso et al., 2007).
Figure 1A, which contains data from the 14 aforementioned
clinical trials, shows more favorable effects of high-frequency
over low-frequency NMES training on functional endurance.
Frontiers in Physiology | www.frontiersin.org 2November 2016 | Volume 7 | Article 544

Veldman et al. Electrical Stimulation and Endurance Performance
FIGURE 1 | (A) Percent improvements in functional endurance after high- and low-frequency neuromuscular electrical stimulation (NMES) interventions in healthy
subjects (gray histograms) and patient populations (black histograms). The numbers above each histogram represent the number of outcome measures the mean
change was computed from, and the mean percent change of these outcome measures. Most of the data, which are not stratified by condition and type of outcome
measure, were extracted from Sillen et al. (2009). Vertical bars denote one standard deviation. (B) Relationship between the total duration of NMES treatment on the
x-axis and NMES training-induced percent improvements in functional endurance in patients suffering from chronic heart failure (CHF) on the y-axis (anecdotally, the
R2is 0.54). Data were obtained from eight different studies published between 2003 and 2006 (Harris et al., 2003; Nuhr et al., 2003; Eicher et al., 2004; Banerjee
et al., 2005; Deley et al., 2005; Dobsák et al., 2006; Karavidas et al., 2006; LeMaitre et al., 2006).
This non-comprehensive analysis is confounded by the disparate
definitions of functional endurance, the absence of stratification
for condition, and the heterogeneity in NMES parameters. For
example, for some unknown reasons, five studies in patients
suffering from COPD used exclusively high-frequency NMES
and showed greater increases in functional endurance (43%)
compared to nine studies conducted in CHF patients that were
administered almost exclusively low-frequency NMES (12%).
Nevertheless, the rate of improvement may also depend on the
severity of the disease. For example, patients with severe CHF
improved more (26%; Nuhr et al., 2003) compared to stable
patients (10%; e.g., Deley et al., 2005) following a low-frequency
NMES training program. More importantly, the total duration
of the NMES treatment (i.e., the training volume) from eight
different studies conducted on CHF patients seems to be
positively related to the magnitude of the improvement in
endurance performance (Figure 1B).
In summary, both high- and low-frequency NMES training
can increase functional endurance in patient populations,
while their influence on muscle endurance is largely unknown
(probably because of the poor clinical relevance of this latter
variable). The impact of NMES training protocols on endurance
performance appears highly dependent on the type of disease, its
severity, and the total exposure to the treatment.
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Veldman et al. Electrical Stimulation and Endurance Performance
CONCLUSIONS
High- and low-frequency NMES training can increase functional
endurance, with the magnitude of the effects being dependent
on the initial condition. That is, inactive patients with advanced
disease are more likely to benefit from NMES training than more
active patients with stable symptoms and healthy individuals.
The most likely explanation for this observation is that the
quadriceps muscle, mostly targeted by NMES, is highly involved
in several activities of daily living and is therefore less sensitive
to improvements in active individuals. We therefore argue that
NMES training is particularly useful for patients that are unable
or unwilling to participate in daily activities or in regular physical
exercise. Despite the heterogeneity of the studies in terms of
study populations, NMES parameters, and outcome measures,
we provide recommendations for clinical use and present ideas
to increase treatment effectiveness. Although recent comparison
studies did not show differences in the acute responses between
high- and low-frequency NMES in both CHF (Sbruzzi et al.,
2010) and COPD patients (Sillen et al., 2011), low-frequency
NMES training seems to be particularly effective for patients with
CHF, with longer treatment durations causing larger increases in
functional endurance (Figure 1B), while for COPD patients, it is
difficult to provide specific recommendations concerning high-
vs. low-frequency NMES due to limited data.
Although the literature has provided us with many
mechanistic and clinical insights into NMES training-induced
effects on muscle and functional endurance, the trials conducted
so far have some methodological limitations and need to be
improved. First, there is a clear distinction between the trials
in healthy participants and those in patient populations. While
studies in healthy individuals focus on mechanistic parameters
such as fiber type composition and capillarization and have few
outcome measures that are clinically relevant, studies in patient
populations merely focus on functional/clinical outcomes. While
such distinctions are understandable from a patient-burden
point of view, the mechanisms underlying NMES-induced
adaptations may differ between diseased and healthy individuals.
Therefore, randomized controlled trials are needed that compare
high- and low-frequency NMES training programs for both
lower and upper extremity muscle groups in patient populations
vs. age- and gender-matched healthy controls. In addition,
because the clinical applicability also depends on whether
NMES-induced effects can still be observed after several months,
follow-up measures should be included in future trials.
In conclusion, we propose here that both high- and
low-frequency NMES training (and probably a combination
of the two, depending on clinicians’ needs) are potentially
relevant to improve endurance performance, and that although
their physiological effects are relatively well understood in
healthy subjects, more evidence-based research is required
to optimize NMES treatment protocols for various patient
populations.
AUTHOR CONTRIBUTIONS
All authors listed, have made substantial, direct and intellectual
contribution to the work, and approved it for publication.
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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.
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Frontiers in Physiology | www.frontiersin.org 5November 2016 | Volume 7 | Article 544