Archivos de Bronconeumología (English Edition) Archivos de Bronconeumología (English Edition)
Arch Bronconeumol 2017;53:357-9 - Vol. 53 Num.7 DOI: 10.1016/j.arbr.2017.01.005
Exercise Training Versus Neuromuscular Stimulation in Severe COPD
Entrenamiento físico frente a estimulación neuromuscular en la EPOC grave
Matthew Maddocksa, Veronica Delogub, Sarah E. Jonesb, Michael I. Polkeyb, William D.-C. Manb,c,,
a King's College London, Cicely Saunders Institute, Londres, United Kingdom
b NIHR Respiratory Biomedical Research Unit, Royal Brompton & Harefield NHS Foundation Trust and Imperial College, Londres, United Kingdom
c Harefield Pulmonary Rehabilitation Unit, Harefield, Middlesex, United Kingdom

Exercise intolerance is a hallmark of severe chronic obstructive pulmonary disease (COPD), resulting from early onset of breathlessness and fatigue on exertion, due in turn to impaired oxygen uptake, reduced cardiovascular fitness and skeletal muscle dysfunction.1 Exercise tolerance can be improved by aerobic and resistance training, which is typically packaged as part of pulmonary rehabilitation. Nonetheless, not everyone may benefit due to issues with poor uptake and completion, particularly in very severe disease2 or following acute exacerbations,3 and response isheterogeneous.2 Furthermore, symptom burden may restrict patients’ ability to perform whole body exercise at the intensity needed to induce meaningful physiological adaptations. Interest in neuromuscular electrical stimulation (NMES) as an alternative training modality in severe COPD has therefore grown steadily since early studies at the turn of the century.4,5 There is now convincing evidence that NMES provides a valid stimulus to cause muscle adaptions,6 and placebo-controlled data support a secondary effect on exercise tolerance.7 But how does NMES compare to classic forms of training? And where might this modality fit in the exercise toolkit when supporting patients with severe disease? Here we consider NMES studies with active comparator, usually another training modality, to begin to understand a role for this modality in practice and suggest possibilities for the next generation of studies in this field.

NMES vs. Resistance or Endurance Training

In the largest comparative effectiveness trial, Sillen et al. randomised patients with severe COPD and lower limb weakness (n=120) to receive either high frequency NMES, low frequency NMES, or resistance training as the exercise component of an 8-week inpatient rehabilitation programme.8 All three groups improved their exercise tolerance when compared to baseline, but quadriceps strength improved only in those allocated to high frequency NMES or resistance training. The lack of effect following low frequency NMES likely reflects an insufficient load being placed on the muscle, which can be difficult to achieve using low frequency currents without concurrent use of high stimulation amplitudes that patients can find uncomfortable. Absolute changes in strength were numerically greater following high frequency NMES than resistance training, though not statistically different between groups. This finding challenges the common assumption that resistance training produces greater muscular adaptation. A training effect from NMES is limited by the discomfort associated with high amplitudes currents applied to the skin plus the early onset of fatigue.9 Contractions achieved with NMES typically equate to 15%–25% of one-repetition maximum,6 although it should be remembered this reflects the periphery of the muscle working maximally and the rest not at all. Whilst this is low compared to what can be achieved with resistance training, it should be borne in mind that the latter has a higher metabolic cost, therefore in severe disease the added exertion may compromise regular training. Indeed, although the resistance training group in the study demonstrated appropriate training progression, and the use of isokinetic testing mimicked the training tasks, only a modest improvement of ∼0.5kg in quadriceps strength was observed.8

There are no data from randomised trials comparing NMES to endurance training, but two observational studies, including a “real-life” evaluation from the clinical setting by Coquart et al.,10 are available. Consecutive patients (n=189) undergoing home-based pulmonary rehabilitation received resistance exercises with free weights, education, and psychosocial support for up to 9 weeks with once-weekly therapist visits. Additionally, patients received either endurance training using a stationary cycle (30–45min 5 times weekly) or NMES (30min, twice daily), which was offered to patients demonstrating poor performance during a step test.10 Whilst the allocation protocol resulted in a better baseline performance among the endurance training group, after the programme similar percentage changes were observed in functional mobility and exercise capacity across cycling and NMES groups, and a similar proportion of responders in terms of overall health status.10 Despite the methodological limitations, this work is a commendable example of how NMES can be integrated into clinical practice. The findings also corroborate an earlier report on a smaller cohort (n=50),11 although the protocol was less explicit on when NMES was selected over endurance training.

NMES as a Training Adjunct

In many international settings, the exercise component of pulmonary rehabilitation is predominantly walking-based and has only a marginal effect on quadriceps strength and mass. Although supervised resistance training augments the overall strengthening effect, access to specialist resistance training equipment may be limited, particularly in the home setting and in low income countries. NMES may therefore have a role as a training adjunct to enhance lower limb muscle mass and function. A randomised pilot study (n=27) from Tasdemir et al. explored whether adding NMES to a 10-week pulmonary rehabilitation programme had additive effects on functional performance.12 There were no significant inter-group differences in quadriceps strength, symptom burden or health status following the programme, but incremental shuttle walk test performance was significantly reduced following active NMES compared to placebo.12 The authors concluded that “increase in exercise capacity is less important when NMES is used as an adjunct to pulmonary rehabilitation”, but this interpretation questions the very hypothesis under investigation. We suggest that the described NMES programme (two 20min sessions each week) offered an inadequate training dose – indeed good evidence of an added strengthening effect was also lacking – and, viewed in this context, the difference in exercise performance may represent a chance finding. An adequately powered study, ideally with measurements to demonstrate a mechanism of action, is justified.

NMES as a Training Precursor

Another role for NMES in severe disease may be as a precursor or bridge to more intense training or pulmonary rehabilitation. Whilst there are no data directly supporting this role, the pragmatic trial by Greening et al.13 in which early rehabilitation following an acute exacerbation did not reduce readmission rates compared to usual care, provides some useful insights. Whilst much of the debate around this study concerns whether the intervention was ‘pulmonary rehabilitation’,14 it is not widely considered a NMES study despite 90% of patients choosing NMES as their core training modality. The short length of hospital stay meant the dose of supervised training was modest (typically 3–4 sessions) and the home component was lightly supervised, resulting in poor adherence.14 Interestingly, uptake of outpatient pulmonary rehabilitation following the trial intervention was higher in the control group (22% vs. 14%), perhaps suggesting that patients in the intervention group may have considered their rehabilitation needs to have been met.13 This is unfortunate, as the post-exacerbation period represents a window of opportunity to engage patients inrehabilitation,3 a notion supported eloquently by a health coaching study by Benzo et al.15 in which pulmonary rehabilitation attendance was enhanced considerably in the 3 months following hospital discharge (50% vs. 33%). Given that patients view NMES as attractive at this time, and can be motivated to enrol for supervised training following recovery, it may serve as an interim measure offered clearly to complement rather than replace pulmonary rehabilitation services.

In summary, based on current evidence, NMES appears to be a reasonable alternative to resistance training if used as part of a comprehensive rehabilitation programme, particularly in advanced disease or where training intensity is limited by exertional symptoms. The lack of high-quality controlled data limits any comparison between NMES with endurance training or the role of NMES as a training adjunct. Further studies, with exercise (rather than muscle) endpoints are required before practical recommendations can be made.


This work was supported by the NIHR Respiratory Biomedical Research Unit at the Royal Brompton and Harefield NHS Foundation Trust and Imperial College, London UK, who partly funded MIP's salary. MM is supported by the NIHR Collaboration for Leadership in Applied Health Research and Care (CLAHRC) for South London and Cicely Saunders International. SEJ is supported by a NIHR Doctoral Fellowship. VD and WD-CM are supported by the NIHR CLAHRC for Northwest London. The views expressed in this publication are those of the authors and not necessarily those of the NHS, The National Institute for Health Research or the Department of Health.

W.D. Man,M.G. Soliman,J. Gearing,S.G. Radford,G.F. Rafferty,B.J. Gray
Symptoms and quadriceps fatigability after walking and cycling in chronic obstructive pulmonary disease
Am J Respir Crit Care Med, 168 (2003), pp. 562-567
M. Maddocks,S.S. Kon,J.L. Canavan,S.E. Jones,C.M. Nolan,A. Labey
Physical frailty and pulmonary rehabilitation in COPD: a prospective cohort study
Thorax, (2016),
M. Maddocks,S.S. Kon,S.J. Singh,W.D. Man
Rehabilitation following hospitalization in patients with COPD: can it reduce readmissions?
Respirology (Carlton, Vic), 20 (2015), pp. 395-404
J.A. Neder,D. Sword,S.A. Ward,E. Mackay,L.M. Cochrane,C.J. Clark
Home based neuromuscular electrical stimulation as a new rehabilitative strategy for severely disabled patients with chronic obstructive pulmonary disease (COPD)
Thorax, 57 (2002), pp. 333-337
G. Bourjeily-Habr,C.L. Rochester,F. Palermo,P. Snyder,V. Mohsenin
Randomised controlled trial of transcutaneous electrical muscle stimulation of the lower extremities in patients with chronic obstructive pulmonary disease
Thorax, 57 (2002), pp. 1045-1049
M. Maddocks,W. Gao,I.J. Higginson,A. Wilcock
Neuromuscular electrical stimulation for muscle weakness in adults with advanced disease
Cochrane Database Syst Rev, 1 (2013), pp. Cd009419
M. Maddocks,C.M. Nolan,W.D. Man,M.I. Polkey,N. Hart,W. Gao
Neuromuscular electrical stimulation to improve exercise capacity in patients with severe COPD: a randomised double-blind, placebo-controlled trial
Lancet Respir Med, 4 (2016), pp. 27-36
M.J.H. Sillen,F.M.E. Franssen,J.M.L. Delbressine,A.W. Vaes,E.F.M. Wouters,M.A. Spruit
Efficacy of lower-limb muscle training modalities in severely dyspnoeic individuals with COPD and quadriceps muscle weakness: results from the DICES trial
N.A. Maffiuletti
Physiological and methodological considerations for the use of neuromuscular electrical stimulation
Eur J Appl Physiol, 110 (2010), pp. 223-234
J.B. Coquart,J.M. Grosbois,C. Olivier,F. Bart,I. Castres,B. Wallaert
Home-based neuromuscular electrical stimulation improves exercise tolerance and health-related quality of life in patients with COPD
Int J Chron Obstruct Pulmon Dis, 11 (2016), pp. 1189-1197
D. Kaymaz,P. Ergun,E. Demirci,N. Demir
Comparison of the effects of neuromuscular electrical stimulation and endurance training in patients with severe chronic obstructive pulmonary disease
Tuberkuloz ve Toraks, 63 (2015), pp. 1-7
F. Tasdemir,D. Inal-Ince,P. Ergun,D. Kaymaz,N. Demir,E. Demirci
Neuromuscular electrical stimulation as an adjunct to endurance and resistance training during pulmonary rehabilitation in stable chronic obstructive pulmonary disease
Expert Rev Respir Med, 9 (2015), pp. 493-502
N.J. Greening,J.E.A. Williams,S.F. Hussain,T.C. Harvey-Dunstan,M.J. Bankart,E.J. Chaplin
An early rehabilitation intervention to enhance recovery during hospital admission for an exacerbation of chronic respiratory disease: randomised controlled trial
BMJ, 349 (2014), pp. g4315
W.D. Man,S.S. Kon,M. Maddocks
Rehabilitation after an exacerbation of chronic respiratory disease
BMJ (Clin Res ed), 349 (2014), pp. g4370
R. Benzo,K. Vickers,P.J. Novotny,S. Tucker,J. Hoult,P. Neuenfeldt
Health Coaching and COPD Re-hospitalization: a randomized study
Am J Respir Crit Care Med, (2016),

Please cite this article as: Maddocks M, Delogu V, Jones SE, Polkey MI, Man WD-C. Entrenamiento físico frente a estimulación neuromuscular en la EPOC grave. Arch Bronconeumol. 2017;53:357–359.

Corresponding author. (William D.-C. Man
Copyright © 2016. SEPAR
Arch Bronconeumol 2017;53:357-9 - Vol. 53 Num.7 DOI: 10.1016/j.arbr.2017.01.005