Editorial
Exercise Training Versus Neuromuscular Stimulation in Severe COPD
Entrenamiento físico frente a estimulación neuromuscular en la EPOC grave
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Jones, Michael I. Polkey, William D.-C. Man" "autores" => array:5 [ 0 => array:3 [ "nombre" => "Matthew" "apellidos" => "Maddocks" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "aff0005" ] ] ] 1 => array:3 [ "nombre" => "Veronica" "apellidos" => "Delogu" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">b</span>" "identificador" => "aff0010" ] ] ] 2 => array:3 [ "nombre" => "Sarah E." "apellidos" => "Jones" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">b</span>" "identificador" => "aff0010" ] ] ] 3 => array:3 [ "nombre" => "Michael I." "apellidos" => "Polkey" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">b</span>" "identificador" => "aff0010" ] ] ] 4 => array:4 [ "nombre" => "William D.-C." "apellidos" => "Man" "email" => array:1 [ 0 => "research@williamman.co.uk" ] "referencia" => array:3 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">b</span>" "identificador" => "aff0010" ] 1 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">c</span>" "identificador" => "aff0015" ] 2 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">*</span>" "identificador" => "cor0005" ] ] ] ] "afiliaciones" => array:3 [ 0 => array:3 [ "entidad" => "King's College London, Cicely Saunders Institute, Londres, United Kingdom" "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:3 [ "entidad" => "NIHR Respiratory Biomedical Research Unit, Royal Brompton & Harefield NHS Foundation Trust and Imperial College, Londres, United Kingdom" "etiqueta" => "b" "identificador" => "aff0010" ] 2 => array:3 [ "entidad" => "Harefield Pulmonary Rehabilitation Unit, Harefield, Middlesex, United Kingdom" "etiqueta" => "c" "identificador" => "aff0015" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0005" "etiqueta" => "⁎" "correspondencia" => "Corresponding author." ] ] ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "Entrenamiento físico frente a estimulación neuromuscular en la EPOC grave" ] ] "textoCompleto" => "<span class="elsevierStyleSections"><p id="par0005" class="elsevierStylePara elsevierViewall">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.<a class="elsevierStyleCrossRef" href="#bib0080"><span class="elsevierStyleSup">1</span></a> 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 disease<a class="elsevierStyleCrossRef" href="#bib0085"><span class="elsevierStyleSup">2</span></a> or following acute exacerbations,<a class="elsevierStyleCrossRef" href="#bib0090"><span class="elsevierStyleSup">3</span></a> and response isheterogeneous.<a class="elsevierStyleCrossRef" href="#bib0085"><span class="elsevierStyleSup">2</span></a> 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.<a class="elsevierStyleCrossRefs" href="#bib0095"><span class="elsevierStyleSup">4,5</span></a> There is now convincing evidence that NMES provides a valid stimulus to cause muscle adaptions,<a class="elsevierStyleCrossRef" href="#bib0105"><span class="elsevierStyleSup">6</span></a> and placebo-controlled data support a secondary effect on exercise tolerance.<a class="elsevierStyleCrossRef" href="#bib0110"><span class="elsevierStyleSup">7</span></a> 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.</p><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0005">NMES vs. Resistance or Endurance Training</span><p id="par0010" class="elsevierStylePara elsevierViewall">In the largest comparative effectiveness trial, Sillen et al. randomised patients with severe COPD and lower limb weakness (<span class="elsevierStyleItalic">n</span>=120) to receive either high frequency NMES, low frequency NMES, or resistance training as the exercise component of an 8-week inpatient rehabilitation programme.<a class="elsevierStyleCrossRef" href="#bib0115"><span class="elsevierStyleSup">8</span></a> 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.<a class="elsevierStyleCrossRef" href="#bib0120"><span class="elsevierStyleSup">9</span></a> Contractions achieved with NMES typically equate to 15%–25% of one-repetition maximum,<a class="elsevierStyleCrossRef" href="#bib0105"><span class="elsevierStyleSup">6</span></a> 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 ∼0.5<span class="elsevierStyleHsp" style=""></span>kg in quadriceps strength was observed.<a class="elsevierStyleCrossRef" href="#bib0115"><span class="elsevierStyleSup">8</span></a></p><p id="par0015" class="elsevierStylePara elsevierViewall">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.,<a class="elsevierStyleCrossRef" href="#bib0125"><span class="elsevierStyleSup">10</span></a> are available. Consecutive patients (<span class="elsevierStyleItalic">n</span>=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 (30–45<span class="elsevierStyleHsp" style=""></span>min 5 times weekly) or NMES (30<span class="elsevierStyleHsp" style=""></span>min, twice daily), which was offered to patients demonstrating poor performance during a step test.<a class="elsevierStyleCrossRef" href="#bib0125"><span class="elsevierStyleSup">10</span></a> 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.<a class="elsevierStyleCrossRef" href="#bib0125"><span class="elsevierStyleSup">10</span></a> 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 (<span class="elsevierStyleItalic">n</span>=50),<a class="elsevierStyleCrossRef" href="#bib0130"><span class="elsevierStyleSup">11</span></a> although the protocol was less explicit on when NMES was selected over endurance training.</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0010">NMES as a Training Adjunct</span><p id="par0020" class="elsevierStylePara elsevierViewall">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 (<span class="elsevierStyleItalic">n</span>=27) from Tasdemir et al. explored whether adding NMES to a 10-week pulmonary rehabilitation programme had additive effects on functional performance.<a class="elsevierStyleCrossRef" href="#bib0135"><span class="elsevierStyleSup">12</span></a> 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.<a class="elsevierStyleCrossRef" href="#bib0135"><span class="elsevierStyleSup">12</span></a> 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 20<span class="elsevierStyleHsp" style=""></span>min 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.</p></span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0015">NMES as a Training Precursor</span><p id="par0025" class="elsevierStylePara elsevierViewall">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.<a class="elsevierStyleCrossRef" href="#bib0140"><span class="elsevierStyleSup">13</span></a> 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’,<a class="elsevierStyleCrossRef" href="#bib0145"><span class="elsevierStyleSup">14</span></a> 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.<a class="elsevierStyleCrossRef" href="#bib0145"><span class="elsevierStyleSup">14</span></a> 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.<a class="elsevierStyleCrossRef" href="#bib0140"><span class="elsevierStyleSup">13</span></a> This is unfortunate, as the post-exacerbation period represents a window of opportunity to engage patients inrehabilitation,<a class="elsevierStyleCrossRef" href="#bib0090"><span class="elsevierStyleSup">3</span></a> a notion supported eloquently by a health coaching study by Benzo et al.<a class="elsevierStyleCrossRef" href="#bib0150"><span class="elsevierStyleSup">15</span></a> 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.</p><p id="par0030" class="elsevierStylePara elsevierViewall">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.</p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0020">Funding</span><p id="par0035" class="elsevierStylePara elsevierViewall">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.</p></span></span>" "textoCompletoSecciones" => array:1 [ "secciones" => array:5 [ 0 => array:2 [ "identificador" => "sec0005" "titulo" => "NMES vs. Resistance or Endurance Training" ] 1 => array:2 [ "identificador" => "sec0010" "titulo" => "NMES as a Training Adjunct" ] 2 => array:2 [ "identificador" => "sec0015" "titulo" => "NMES as a Training Precursor" ] 3 => array:2 [ "identificador" => "sec0020" "titulo" => "Funding" ] 4 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "NotaPie" => array:1 [ 0 => array:2 [ "etiqueta" => "☆" "nota" => "<p class="elsevierStyleNotepara" id="npar0005">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.</p>" ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0005" "bibliografiaReferencia" => array:15 [ 0 => array:3 [ "identificador" => "bib0080" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Symptoms and quadriceps fatigability after walking and cycling in chronic obstructive pulmonary disease" "autores" => array:1 [ 0 => array:2 [ "etal" => true "autores" => array:6 [ 0 => "W.D. Man" 1 => "M.G. Soliman" 2 => "J. Gearing" 3 => "S.G. Radford" 4 => "G.F. Rafferty" 5 => "B.J. 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| Year/Month | Html | Total | |
|---|---|---|---|
| 2024 November | 5 | 4 | 9 |
| 2024 October | 98 | 24 | 122 |
| 2024 September | 57 | 26 | 83 |
| 2024 August | 89 | 43 | 132 |
| 2024 July | 63 | 22 | 85 |
| 2024 June | 70 | 27 | 97 |
| 2024 May | 113 | 32 | 145 |
| 2024 April | 61 | 25 | 86 |
| 2024 March | 51 | 15 | 66 |
| 2024 February | 31 | 20 | 51 |
| 2023 March | 12 | 4 | 16 |
| 2023 February | 61 | 19 | 80 |
| 2023 January | 24 | 31 | 55 |
| 2022 December | 60 | 23 | 83 |
| 2022 November | 74 | 27 | 101 |
| 2022 October | 57 | 38 | 95 |
| 2022 September | 31 | 30 | 61 |
| 2022 August | 28 | 45 | 73 |
| 2022 July | 29 | 34 | 63 |
| 2022 June | 33 | 20 | 53 |
| 2022 May | 36 | 40 | 76 |
| 2022 April | 53 | 40 | 93 |
| 2022 March | 38 | 41 | 79 |
| 2022 February | 38 | 18 | 56 |
| 2022 January | 65 | 43 | 108 |
| 2021 December | 47 | 48 | 95 |
| 2021 November | 40 | 39 | 79 |
| 2021 October | 78 | 53 | 131 |
| 2021 September | 35 | 40 | 75 |
| 2021 August | 42 | 38 | 80 |
| 2021 July | 58 | 21 | 79 |
| 2021 June | 36 | 28 | 64 |
| 2021 May | 38 | 26 | 64 |
| 2021 April | 97 | 77 | 174 |
| 2021 March | 50 | 31 | 81 |
| 2021 February | 26 | 22 | 48 |
| 2021 January | 31 | 15 | 46 |
| 2020 December | 31 | 17 | 48 |
| 2020 November | 42 | 26 | 68 |
| 2020 October | 27 | 21 | 48 |
| 2020 September | 25 | 14 | 39 |
| 2020 August | 32 | 12 | 44 |
| 2020 July | 25 | 21 | 46 |
| 2020 June | 20 | 9 | 29 |
| 2020 May | 29 | 16 | 45 |
| 2020 April | 43 | 24 | 67 |
| 2020 March | 49 | 11 | 60 |
| 2020 February | 46 | 25 | 71 |
| 2020 January | 48 | 17 | 65 |
| 2019 December | 65 | 22 | 87 |
| 2019 November | 46 | 39 | 85 |
| 2019 October | 36 | 18 | 54 |
| 2019 September | 28 | 8 | 36 |
| 2019 August | 21 | 18 | 39 |
| 2019 July | 24 | 18 | 42 |
| 2019 June | 29 | 19 | 48 |
| 2019 May | 29 | 36 | 65 |
| 2019 April | 32 | 56 | 88 |
| 2019 March | 54 | 28 | 82 |
| 2019 February | 27 | 18 | 45 |
| 2019 January | 27 | 22 | 49 |
| 2018 December | 32 | 19 | 51 |
| 2018 November | 43 | 27 | 70 |
| 2018 October | 54 | 28 | 82 |
| 2018 September | 25 | 8 | 33 |
| 2018 May | 13 | 0 | 13 |
| 2018 April | 21 | 8 | 29 |
| 2018 March | 59 | 8 | 67 |
| 2018 February | 67 | 12 | 79 |
| 2018 January | 63 | 11 | 74 |
| 2017 December | 46 | 13 | 59 |
| 2017 November | 37 | 13 | 50 |
| 2017 October | 36 | 18 | 54 |
| 2017 September | 1 | 1 | 2 |
| 2017 June | 0 | 1 | 1 |
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