Effects of neuromuscular electrical stimulation on exercise capacity,muscle strength and quality of life in COPD patients: A Systematic Review with Meta-Analysis

Abstract

Objective

To determine the effects of neuromuscular electrical stimulation on disabilities and activity limitation of individuals affected by chronic obstructive pulmonary disease.

Data sources

MEDLINE, PEDro database, Cochrane Controlled Trials Register, and SciELO, were searched from inception until October 2021.

Review methods

Inclusion criteria were patients with COPD, randomized controlled trials comparing neuromuscular electrical stimulation alone or combined conventional pulmonary rehabilitation and neuromuscular electrical stimulation versus control or sham or pulmonary rehabilitation in disabilities and activity limitation in COPD. There were no mandatory language or publication date restrictions. Two reviewers selected studies independently. Weighted mean differences and 95% confidence intervals were calculated. Results 32 studies met the study criteria, including 1.269 participants. Neuromuscular electrical stimulation improved exercise capacity (MD 1.10, 95% CI: 0.33, 1.86, N = 147), and muscle strength (0.53, 95% CI: 0.20, 0.87, N = 147) compared to sham group. Combined neuromuscular electrical stimulation and conventional rehabilitation improved exercise capacity (MD 34.28 meters, 95% CI: 6.84, 61.73, N = 262) compared to conventional rehabilitation alone. No adverse events were reported.

Conclusions

Neuromuscular electrical stimulation resulted in small improvement in disabilities and activity limitation (below the MCID) in COPD. Thus, the inclusion of neuromuscular electrical stimulation in rehabilitation programs must consider the cost Because of inadequate methodological conduction and reporting of methods, some studies were of low quality.

Keywords

COPD neuromuscular electrical stimulation rehabilitation

Introduction

Chronic obstructive pulmonary disease is a major cause of chronic disability and mortality worldwide.¹ In individuals with chronic obstructive pulmonary disease, highlight the impairment in skeletal muscle function and mass, particularly of the limb muscles² and is a major contributor to exercise limitation, quality of life impairment, and is an independent predictor of morbidity and mortality.^2–4

New modalities of rehabilitation techniques in disabilities and activity limitation in chronic obstructive pulmonary disease have been rising in the literature as an alternative to optimize adherence and clinical outcomes, such as muscle weakness and exercise tolerance. Neuromuscular electrical stimulation may be an effective treatment for muscle weakness in adults with advanced progressive disease.^5–8

Systematic review that investigates the role of neuromuscular electrical stimulation in disabilities and activity limitation in chronic obstructive pulmonary disease patients have been published.^9–11 However, the previous reviews have not reached consistent conclusions.^9–11 In addition, these reviews performed the search in December of 2012, June of 2016 and May 2018 and new studies have been completed and published since then.^9–11

The aim of this systematic review was to analyze the published randomized controlled trials that investigated the effects of neuromuscular electrical stimulation alone or combined neuromuscular electrical stimulation and conventional rehabilitation on disabilities and activity limitation of individuals affected by chronic obstructive pulmonary disease.

Methods

The review was planned and conducted in accordance with PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) guidelines.¹² The last search was October 2021.

This systematic review included all RCTs that studied the effects of neuromuscular electrical stimulation alone or combined neuromuscular electrical stimulation and conventional rehabilitation in chronic obstructive pulmonary disease patients. Studies were considered for inclusion regardless language or publication date. Trials enrolling adults with chronic obstructive pulmonary disease were included in this systematic review. To be eligible, the trial should have randomized chronic obstructive pulmonary disease patients to, at least, one group of neuromuscular electrical stimulation.

We searched for references on MEDLINE, PEDro database, and the Cochrane Controlled Trials Register, and SciELO. A standard protocol for this search was developed and controlled vocabulary was used. Key words and their synonymous were used to sensitize the search. For the identification of RCTs was used the strategy developed for the Cochrane Collaboration.¹³ In the search strategy, there were three groups of keywords: study design, participants, and interventions (Supplementary material – S1). Checking reference lists to detect potentially eligible studies. The authors were contacted by e-mail for ongoing studies or when additional information was needed.

Two authors independently, IGNA and MGN, evaluated each abstract and full text article identified in the research for eligibility and filled inclusion and exclusion criteria in a standard form. If at least one of the authors considered one reference eligible, the full text was obtained for complete assessment.

Two authors independently, IGNA and MGN, extracted data (standardized data extraction) from the published reports using standard data extraction forms adapted from the Cochrane Collaboration's¹³ model for data extraction, considering: average age and sex, sample size, frequency, intensity, pulse duration, duty cycle, and duration of each session, follow-up, loss to follow-up, outcome measures and presented results. In case of any disagreement, the authors discussed, and a final decision was made by consensus.

Additionally, two researchers independently assessed methodological quality. Studies were scored on the PEDro scale¹⁴ based on a Delphi list.¹⁵ One item on the PEDro scale (eligibility criteria) is related to external validity and is generally not used to calculate the method score, leaving a score range of 0 to 10.¹⁵ Any disagreements were resolved by a third rater.

The quality of the evidence for each outcome was performed using the GRADE system. The GRADE approach describes the process of rating the quality of the best available evidence based on five considerations (study limitations, consistency of effect, imprecision, indirectness, and publication bias). The GRADE system uses the following criteria for assigning grade of evidence (high, moderate, low, very low). We decreased grade if: serious (−1) or very serious (−2) limitation to study quality; important inconsistency (−1); some (−1) or major (−2) uncertainty about directness; imprecise or sparse data (−1); high probability of reporting bias (−1).

In accordance with analysis performed by Gomes-Neto 2014,¹⁶ pooled-effect estimates were obtained by comparing the least square mean change from baseline to endpoint for each group and were expressed as the weighted mean difference between groups. Due to the difference between some instruments used, we performed a meta-analysis with standardized mean difference. When the standard deviation (SD) of change was not available, the SD of the baseline measure was used for the meta-analysis. Calculations were done using a random or fixed-effects model based on heterogeneity. Two comparisons were made: neuromuscular electrical stimulation versus control and combined neuromuscular electrical stimulation and conventional rehabilitation versus conventional rehabilitation. Additionally, planned subgroup analyses were conducted based on the local rehabilitation. Subgroup analyses were performed using pre-specified subgroups that included home-based and rehabilitation center. An α value of 0.05 was considered significant. Statistical heterogeneity of the treatment effect among studies was assessed using Cochran's Q-test and the inconsistency I² test, in which values above 30% were considered indicative of high heterogeneity and random-effects model was chosen.¹⁷ Analyses were performed using Review Manager Version 5.3 (Cochrane Collaboration).¹⁸

Results

The initial search led to the identification of abstracts, from which 32 studies were considered as potentially relevant and were retrieved for detailed analysis. Figure 1 shows the PRISMA flow diagram of studies in this review.

Of the 32^19–50 randomized clinical trials included in this review, nine were on neuromuscular electrical stimulation alone compared to a control or sham, from which six performed neuromuscular electrical stimulation in clinical setting and three performed in home. Twelve studies were on combined neuromuscular electrical stimulation and conventional rehabilitation (pulmonary rehabilitation or physical therapy) compared to conventional rehabilitation, from which eleven performed neuromuscular electrical stimulation in clinical setting and one performed in home. One study analyzed the effect of the quadriceps functional Electrical Stimulation-Cycling compared to placebo FES-cycling.

Another study compared neuromuscular electrical stimulation with high-frequency to neuromuscular electrical stimulation with low-frequency. One more compared active limb mobilization with or without electrical stimulation. A further one compared electrical stimulation combined with exercise compared to electrical stimulation in patients receiving mechanical ventilation support.

Additionally, one compared pulmonary rehabilitation plus electrical stimulation on quadriceps and triceps sural compared to pulmonary rehabilitation plus electrical stimulation on quadriceps alone. Another evaluated to active extremity exercise training plus neuromuscular electrical stimulation versus neuromuscular electrical stimulation alone and versus active extremity exercise training and another study compared to neuromuscular electrical stimulation with endurance training. A further one compared neuromuscular electrical stimulation plus aerobic versus control versus neuromuscular electrical stimulation plus Calystenic exercise.

The final sample was 1.269 participants (ranged from 11³⁸ to 389²⁸), and mean age of participants ranged 56.3²⁶ to 76⁴⁴ years. Except for two study,^26,49 all others included patients of both genders, but there was a predominance of male. Patient's gender was not informed in three studies.^42,43,46 The studies analyzed in this systematic review included outpatients with documented moderate to severe chronic obstructive pulmonary disease patients, and all patients were on optimal medical therapy for chronic obstructive pulmonary disease before enrollment. Table 1 summarizes the participants included, sample size, outcomes and results of included studies.

Table 1.

Characteristics of the included studies.

			Intervention groups
	Study	Patients (diagnosis, N analysed, age, gender)	Treatment	Control	Outcome measures	Results
1	Acheche et al. 2020	Moderate to severe Chronic obstructive pulmonary disease, 42 analyzed, 63 years, 42 males	CR + NMES	CR (ET + RT)	TUG, BBS, 6MWT and MVC	The ET + RT + NMES group showed better improvement than the ET + RT group in terms of 6MWD, TUG and MVC
2	Mekki et al. 2019	Chronic obstructive pulmonary disease, 45 analyzed, 59.5 years, 45 males	NMES + PR	PR	Stabilometry, TUG, Berg, 6MWT, MVC	6MWT, TUG, Berg, and MVC were improved in experimental group.
3	Chen et al. 2019	Intubated Chronic obstructive pulmonary disease, 56 analyzed, xx years, xx males	NMES	CTR	MRC-Score, grip strength, incidence of ICU-AW, modified Barthel index score, duration of mechanical ventilation, the length of ICU stay and hospital stay	NMES improved to MRC score, Barthel index and grip strength compared to control. Incidence rate of ICU-AW and length of ICU stay and hospital stay was decreased compared to control.
4	Medrinal et al. 2018	Moderate to severe Chronic obstructive pulmonary disease, 23 analyzed, 63.3 years, 14 males	NMES + Cycling	SHAM + Cycling	VO2, VCO2, VE, Lactate level, dyspnea (Borg scale) and fatigue (visual analogue scale).	Mean VO2, VCO2 and VE were increased using FES + cycling compared to SHAM.
5	Bonnevie et al. 2018	Very severe Chronic obstructive pulmonary disease, 51 analyzed, 59.2 years, 44 males	Home base NMES + PR	PR	6MWT distance, VO2 peak, SGRQ, maximal workload during CPET	There were significant increases in 6MWT, VO2peak, CPET, mMRC and SGRQ total score in NMES group.
6	Péran et al. 2018	Severe to very severe Chronic obstructive pulmonary disease, 11 analyzed, 63,3 years, 6 males	PR + QDC NMES	PR + QDC and triceps surae NMES	MVC, 6MWT, mMRC, Step test	No differences between groups were observed.
7	Valenza et al. 2017	Severe Chronic obstructive pulmonary disease, 36 analyzed, 69 years, 23 males	NMES + PR	MT	6MWT distance, 5-STS, LCADL, CAT	Improvement in 6MWT distance and 5-STS and reduce CAT score, LCADL physical activity subscore and total score in treatment group.
8	Lopez et al. 2017	Moderate to severe hospitalized Chronic obstructive pulmonary disease, 39 analyzed, 63 years, 31 males	NMES + aerobic	CTR X NMES + Calystenic	5-STS test, LCADLS, spirometry, palmar dynamometry, FSS.	NMES + Calystenic group showed better improvement in 5-STS and fatigue compared to all groups. NMES + aerobic and NMES + Calystenic groups showed better improvement in 5-STS and fatigue compared to CTR group.
9	Kucio et al. 2016	Chronic obstructive pulmonary disease, 28 analyzed, 68.3 years, 21 males	NMES + PR	PR	6MWT, spirometric test (FEV1, FVC, FEV1/FVC and PEF) and gasometric test (PO2 and PCO2)	A significant increase of distance walked in the 6MWT was observed only in the NMES + PR group.
10	Maddocks et al. 2016	Severe Chronic obstructive pulmonary disease, 52 analyzed, 69,5 years, 21 males	NMES	SHAM	6MWD, QMVC, RFCSA, EuroQol 5-dimension, SGRQ, CRQ.	Significantly improvement in 6MWT distance, QMVC, RFCSA at NMES group compared to SHAM group.
11	Dolmage et al. 2016	Moderate to severe Chronic obstructive pulmonary disease, 11 analyzed, 62 years, NI males	NMES	SHAM	Strength and endurance	Increased in strength and endurance in intervention group
12	Tasdemir et al. 2015	Moderate to severe Chronic obstructive pulmonary disease, 27 analyzed, 62.5 years, 24 males	NMES + cPR	SHAM + cPR	MRC, FSS, SGRQ, HADS, exercise capacity [ISWT and ESWT) and QDC strength and endurance	NMES + cPR group exhibited higher increases in ISWT and % ISWT distance compared to SHAM + cPR group.
13	Akar et al. 2015	Severe to very severe intubated Chronic obstructive pulmonary disease, 30 analyzed, 66.9 years, 15 males	AAET + NMES	NMES X AAET	Muscle strengths, mobilization duration and weaning situation were evaluated	Lower and upper extremity muscle-strength was significantly improved in AEET + NMES and NMES alone.
14	Tardif et al. 2015	Moderate to severe Chronic obstructive pulmonary disease, 52 analyzed, 59.9 years, 20 males	NMES + PT	PT	SGRQ, 6MWT, mMRC,Wmax, BODEi.	6MWT, BODEi and dyspnea were improved in experimental group.
15	Vieira et al. 2014	Moderate to severe Chronic obstructive pulmonary disease, 20 analyzed, 56.3 years, 20 males	NMES + PT	PT	Tlim, FEV1, FEV1/FVC, peak VO2, SGRQ, 6MWT.	NMES increased FEV1, FEV1/FVC, 6MWD and Tlim when compared to PT group.
16	Sillen et al. 2014	Severe Chronic obstructive pulmonary disease, 24 analyzed, 66 years, 14 males	Hf-NMES	Lf-NMES X Strenght Training	QDC function in Isokinetic (peak torque and total work), 6MWD, CWRT, VO2, VE and SpO2	6MWD, isokinetic quadriceps peak torque and isokinetic total work increased in Hf-NMES.
17	Greening et al. 2014	Severe to very severe Chronic obstructive pulmonary disease, 389 analyzed, 71.1 years, 173 males	Early PR + NMES	PT	Readmissions to hospital, Spirometry, ISWT, ESWT, MVC to QDC	ESWT was significantly higher in the NMES group at six weeks.
18	Akinlabi et al. 2013	Severe Chronic obstructive pulmonary disease, 10 analyzed, 76 years, 5 males	NMES + EXT	EXT	SGRQ, 6MWT, LCADL, HADS	There were no significant differences between-group in the 6MWT, SGRQ or HADS. Significant improvement in LCADL in experimental group.
19	Latimer et al. 2013	Stable Chronic obstructive pulmonary disease, 16 analyzed, 64.5 years, 8 males	NMES	Untrained contralateral limb	QMVC and thigh lean mass	NMES improved the QMVC and thigh lean mass.
20	Vivodtzev et al. 2012	Moderate to severe Chronic obstructive pulmonary disease, 20 analyzed, 69 years, 13 males	Home base NMES	SHAM	Pulmonary function, CSA of CM, QDC strength (MVC) and ESWT.	NMES increased midthigh and CSA of CM and quadriceps strength and endurance and walking distance in ESWT.
21	Zanotti et al. 2012	Moderate Chronic obstructive pulmonary disease, 83 analyzed, 61,7 years, 23 males	NMES + PR	Sham + PR	1MSTST, 6MWT, Lung function, mMRC and SGRQ	NMES improve significantly 6WMT and 1MSTST compared to control group.
22	DalĺAcqua et al. 2012	Moderate to severe Chronic obstructive pulmonary disease, 21 analyzed, 69.7 years, 8 males	NMES + PT	PT	MIP and MEP	NMES + PT increase MIP and MEP compared to PT group.
23	Giavedoni et al. 2012	Chronic obstructive pulmonary disease, 11 analyzed, 72.2 years, 5 males	NMES (treatment leg)	Contralateral leg	BMI, spirometry, QMVC	NMEs promoted increase statistically significant in ΔQMVC compared to CTR group.
24	Abdellaoui et al. 2011	Severe chronic obstructive pulmonary disease exacerbation, 15 analyzed, 63 years, 13 males	NMES	SHAM	MVC, 6MWD and MRC.	MVC and 6MWD were improved in NMES group compared to SHAM.
25	Napolis et al. 2011	Moderate to severe chronic obstructive pulmonary disease, 30 analyzed, 63.7 years, 26 males	Home base High frequency NMES	SHAM	FEV1, FVC, 6MWD, body composition, Tlim, VO2 max, isokinetic knee strength assessment.	No differences, between groups to 6MWD and isokinetic strength.
26	Dang et al. 2011	Moderate to severe chronic obstructive pulmonary disease, 16 analyzed, NI years, NI males	PR + NMES	PR	QDC strength ans endurance, VO2 max, maximal work, quality of life and 6MWD	PR + NMES increased QDC strenght, quality of life and 6MWD compared to PR group.
27	Dal Corso et al. 2007	Moderate to severe Chronic obstructive pulmonary disease, 17 analyzed, 65,9 years, 16 males	NMES	SHAM	Peripheral muscle strength (isokinetic), CSA of VL and 6MWD	No differences were observed between groups to peak torque, muscle mass and 6MWD. NMES was associated with increased in type II fibre CSA.
28	Vivodtzev et al. 2006	Moderate to severe Chronic obstructive pulmonary disease, 17 analyzed, 63,5 years, 11 males	NMES + PT	PT	FEV1 and FVC, MRF-28, QDC strength (MVC) and QDC composition (CTC, QST and ma-MM) and 6MWT	NMES increased MVC. No difference was observed to 6MWD between groups.
29	Gigliotti et al. 2004	Severe Chronic obstructive pulmonary disease, 20 analyzed, NI years, NI males	NMES + EXT	EXT	6MWT, cEnd, dyspnea, SGRQ, and quadriceps strength by an isokinetic dynamometer	NMES group showed a significant increase in quadriceps strength and endurance.
30	Zanotti et al. 2003	Moderate to severe Chronic obstructive pulmonary disease, 24 analyzed, 65.4 years, 17 males	NMES + ALM	ALM	Cardiorespiratory function (Sat, HR, and RR).	ALM + NMES improved n muscle strength and Sat, compared to ALM group.
31	Neder et al. 2002	Moderate to severe Chronic obstructive pulmonary disease, 15 analyzed, 65,8 years, 13 males	Home base High frequency NMES	CTR	CRDQ, peak VO2, knee strength and endurance (isokinetic)	NMES increased peak torque and peak VO2 and reduced muscle fatigue and improved CRDQ score (in dyspnoea domain).
32	Bourjeily-Habr et al. 2002	Moderate to severe Chronic obstructive pulmonary disease, 18 analyzed, 60 years, 10 males	NMES	SHAM	QDC and HM maximal isokinetic strengths ISWT, VO2, MIP, MEP, FEV1, FVC, FEV1/FVC).	QDC and HM strength and ISWD were improved in NMES group when compared to SHAM.

6MWT: six minute walk test; ET: endurance training; SGRQ: Saint George's Respiratory Questionnaire; MIP: maximum inspiratory pressure; MEP: maximum expiratory pressure; QMVC: quadriceps maximal voluntary contraction; MVC: Maximal voluntary contraction; MRC: Medical Research Council; mMRC: modificated Medical Research Council; CSA: cross sectional area; FEV1: forced expiratory volume in 1 s; FVC: forced capacity vital; FEV1/FVC ratio: forced expiratory volume in 1 s and forced capacity vital ratio; VO2 max: maximal oxygen consumption; VCO2: carbon dioxide production; cEnd: cycloergometer endurance; RFCSA: rectus femoris cross-sectional area; CRQ: Chronic Respiratory Questionnaire; QDC: quadriceps; EXT: exercise training; ALM: Active Limb Mobilization; HM: hamstring; VL: vastus lateralis; RF: rectus femoris; Tlim: time to exercise intolerance; CM: calf muscle; CRDQ: Health related quality of life; MRF-28: Quality-of-Life Questionnaire; CTC: corrected thigh circumference; QST: quadriceps skin fold thickness; CWRT: constant work-rate cycling endurance test; VE: minute volume; ISWT: incremental shuttle walk test; SWT: shuttle walk test; ESWT: endurance shuttle walk test; Sat: saturation; 5-STS: five-times-sit to stand; LCADL: London Chest Activity of daily living scale; CPET: Cardiopulmonary exercise testing; MT: medical treatment; PT: physical therapy; PR: pulmonary rehabilitation; cPR: comprehensive pulmonary rehabilitation; AAET: active extremity exercise training; BMI: Body mass index; BIA: bioelectrical impedance analysis; MMT: Manual muscle testing; HADS: Hospital Anxiety and Depression Scale; ICU-AW: intensive care unit-acquired weakness; MRC-Score: Medical Research Council muscle strength score; FSS: Fatigue Severity Scale; 1MSTST:1 minnute Sit to Stand Test.

Twenty-five RCTs included in this review were evaluated by PEDro scale. PEDro scores ranged from 3–7 out of 10 (Table 2). Lower scores were mainly due to lack of blinding of patients, therapists or assessors and not conducting analyses with intention to treat when appropriate. Only one article blinded therapists. Thus, because of inadequate reporting of methods, some studies were of low quality. The quality of the evidence using GRADE comparing was low or very low for all outcomes. It was downgraded the quality of evidence ratings predominantly due to inconsistency among study findings and bias risk (Tables 3 and 4). (Table 5)

Table 2.

Study quality on the PEDro scale.

	Study	1*	2	3	4	5	6	7	8	9	10	11	Total
1	Acheche et al. 2020	✓	✓		✓				✓	✓	✓	✓	6
2	Mekki et al. 2019		✓	✓	✓						✓	✓	5
3	Medrinal et al. 2018	✓	✓	✓	✓				✓		✓	✓	6
4	Bonnevie et al. 2018	✓	✓	✓	✓						✓	✓	5
5	Péran et al. 2018	✓	✓	✓					✓				3
6	Valenza et al. 2017	✓	✓		✓			✓	✓		✓	✓	6
7	Lopez et al. 2017	✓	✓		✓				✓		✓	✓	5
8	Kucio et al. 2016	✓	✓		✓				✓		✓	✓	5
9	Maddocks et al. 2016	✓	✓	✓	✓			✓	✓	✓	✓	✓	8
10	Tasdemi et al. 2015		✓	✓	✓						✓	✓	5
11	Akar et al. 2015	✓	✓		✓			✓			✓	✓	5
12	Vieira et al. 2014	✓	✓		✓						✓	✓	4
13	Sillen et al. 2014		✓		✓	✓	✓	✓	✓		✓	✓	8
14	Greening et al. 2014	✓	✓	✓	✓			✓	✓	✓	✓	✓	8
15	Vivodtzev et al. 2012		✓		✓	✓		✓	✓		✓	✓	7
16	Zanotti et al. 2012	✓	✓								✓	✓	3
17	DalĺAcqua et al. 2012	✓	✓	✓	✓				✓		✓	✓	6
18	Giavedoni et al. 2012	✓	✓						✓		✓	✓	4
19	Abdellaoui et al. 2011	✓	✓		✓				✓		✓	✓	5
20	Napolis et al. 2011	✓	✓			✓		✓	✓		✓	✓	6
21	Dal Corso et al. 2007	✓	✓		✓	✓			✓		✓	✓	6
22	Vivodtzev et al. 2006	✓	✓		✓				✓		✓	✓	5
23	Zanotti et al. 2003	✓	✓		✓						✓	✓	4
24	Neder et al. 2002	✓	✓	✓	✓				✓	✓	✓	✓	7
25	Bourjeily-Habr et al. 2002	✓	✓			✓		✓	✓		✓	✓	6

1: eligibility criteria and source of participants; 2: random allocation; 3: concealed allocation; 4: baseline comparability; 5: blinded participants; 6: blinded therapists;7: blind assessors; 8: adequate follow-up; 9: intention-to-treat analysis; 10: between-group comparisons; 11: point estimates and variability.

*Item 1 does not contribute to the total score.

Table 3.

Summary of findings for the main comparison. NMES + CR compared to conventional rehabilitation for COPD.

Outcomes	Ilustrative comparative risks*(95%IC)		No of participants (studies)	Quality of the evidence (GRADE)	Comments
	Assumed risk	Corresponding risk
	Control	NMES (provided in addition to conventional rehabilitation)
Exercise capacity (6MWT)	CR	The MD walking in the intervention group was 35.1 meters (5.56 lower to 64.66 higher)	220 (6 studies)	⊕⊝⊝⊝ very low^a,b,c,d	Four studies without allocation concealment. All research without blinding of therapists. High heterogeneity. No study reported use of intention-to-treat analysis.
Muscle strength	—	—	—	—	Not measured in the studies
Quality of life	CR	No significant benefit found on total score of the SGRQ	130 (3 studies)	⊕⊕⊝⊝ low^a,d	No statistically significant difference between groups.All research without blinding of therapists.No study reported use of intention-to-treat analysis.

NMES + CR compared to conventional therapy for COPD.

Patient or population: COPD patients.

Settings: clinic or home.

Intervention: NMES + CR.

Comparison: conventional rehabilitation (CR).

CR: conventional rehabilitation; CI: confidence interval; MD: mean difference.

GRADE Working Group grades of evidence.

High quality: we are very confident that the true effect lies close to that of the estimate of the effect.

Moderate quality: we are moderately confident in the effect estimate; the true effect is likely to be close to the estimate of effect, but there is a possibility that it is substantially diferente.

Low quality: our confidence in the effect estimate is limited; the true effect may be substantially different from the estimate of the effect.

Very low quality: we have very little confidence in the effect estimate; the true effect is likely to be substantially different from the estimate of effect.

Risk of bias high in a number of studies.

Downgraded by 1 due to inconsistency in findings across studies.

Surrogate outcome.

Small total population size (< 300).

*The basis for the assumed risk (e.g. the median control group risk across studies) is provided in footnotes. The corresponding risk (and its 95% confidence interval) is based on the assumed risk in the comparison group and the relative effect of the intervention (and its 95% CI).

Table 4.

Summary of findings for the main comparison. NMES compared to SHAM for COPD.

Outcomes	Ilustrative comparative risks*(95%IC)		N° of participants (studies)	Quality of the evidence (GRADE)	Comments
	Assumed risk	Corresponding risk
	Control	NMES (provided in addition to conventional rehabilitation)
Exercise capacity (6MWT)	CR	SMD to exercise capacity was significantly higher among treated patients with NMES compared to patients in the sham group (1.10, 95% CI: 0.33, 1.86	147 (6 studies)	⊕⊝⊝⊝ very low^a^,^b^,^c^,^d	One study without eligibility criteria and source of participants. Five studies did not performed concealed allocation. All research without blinding of therapists.
Muscle strength	CR	The SMD to muscle strength was significantly higher among treated patients with NMES compared to patients in the sham group (0.53, 95% CI: 0.19, 0.88	147 (6 studies)	⊕⊝⊝⊝ very low ^a^,^b^,^c^,^d	Five studies did not performed concealed allocation. All research without blinding of therapists. Only one study reported use of intention-to-treat analysis
Quality of life	—	—	—	—	Not measured in the studies

NMES compared to SHAM.

Patient or population: COPD patients.

Settings: clinic or home.

Intervention: NMES.

Comparison: SHAM.

CR: conventional rehabilitation; CI: confidence interval; MD: mean difference; RR: risk ratio; SMD: standardised mean difference.

GRADE Working Group grades of evidence.

High quality: we are very confident that the true effect lies close to that of the estimate of the effect.

Moderate quality: we are moderately confident in the effect estimate; the true effect is likely to be close to the estimate of effect, but there is a possibility that it is substantially diferente.

Low quality: our confidence in the effect estimate is limited; the true effect may be substantially different from the estimate of the effect.

Very low quality: we have very little confidence in the effect estimate; the true effect is likely to be substantially different from the estimate of effect.

Risk of bias high in a number of studies.

Downgraded by 1 due to inconsistency in findings across studies.

Surrogate outcome.

Small total population size (< 300).

Table 5.

Characteristics of the experimental intervention) the trials included in the review.

N	Study, year	Intensity	Current	Frequency	Muscles and Electrodes	Pulse Width (ms)	Duty cycle (Ton/Toff) (s)	Time (min/d)	Frequency (x/wk)	Duration (wk)
1	Acheche 2020	maximal contraction to be produced	Symmetrical Biphasic	50 Hz	QDC/CM and 16 rectangular electrodes (5 × 5 cm2)	400 ms	10/30	NI	3	24
2	Mekki et al. 2019	15 a 60 mA	NI	50 Hz	QDC, SMT, SMM and NI	400 ms	5/15	20	3	24
3	Chen et al. 2019	NI	NI	NI	NI	NI	NI	30	2	Until ICU discharge
4	Medrinal et al. 2018	Visible contraction	Rectangular intermittent bidirectional	35 Hz	QDC and electrodes (5 × 9 cm)	300 ms	NI	30	NI	NI
5	Bonnevie et al. 2018	Maximal tolerated	Symmetrical Biphasic	35 Hz	QDC and electrodes 10 × 5 cm or 5 × 5 cm	400 ms	0.5/1.5	30	5	8
6	Perán et al. 2018	Maximal tolerated	Symmetrical Biphasic	50 Hz	QDC/Triceps sural and 4 electrodes (5 × 5 cm)	350 ms	6s/6	30	5	4
7	Lopez et al. 2017	Maximal tolerated	Assymmetrical Biphasic	50 Hz	QDC and NI	400 ms	8/20	30	Daily	Until hospital discharge
8	Valenza et al. 2017	Visible contraction	Asymmetrical Biphasic	50 Hz	QDC and NI	400 ms	8/20	15	2	8
9	Kucio et al. 2016	NI	Symmetric retangular	35 Hz	QDC/GM and NI	0.3 ms	2/4	NI	6	3
10	Maddocks et al. 2016	15–25% of a maximum voluntary contraction	Biphasic	50 Hz	QDC and electrodes (10 × 13 cm)	350 ms	2:15 to 5:20 to 10:15 increased on a weekly	30	7	6
11	Dolmage et al. 2016	Maximal tolerated.	NI	15 Hz	QDC and NI	NI	10/50	60	5	6
12	Tasdemi et al. 2015	Maximal tolerated.	Symmetrical Biphasic	50 Hz	QDC and Two rectangular electrodes (9 × 5 cm)	300 ms	10/20	20	2	10
13	Akar et al. 2015	Intensity was set to create a visible contraction	Symmetrical biphasic	50 Hz	QDC/deltoid and electrodes (9 × 5 cm)	NI	1.5/0.75	NI	daily	4
14	Tardif et al. 2015	Intensity set to obtain a maximal stimulation without pain	NI	35 Hz	QDC and NI	NI	NI	30	5	8
15	Vieira et al. 2014	Maximal tolerated.	Symmetrical Biphasic	50 Hz	QDC and NI	300–400 ms	2/18 to 5/25 to 10/30	60	5	8
16	Sillen et al. 2014	NI	NI	75 Hz (HF) and 15 HZ (LF)	QDC and NI	NI	NI	NI	5 times per week and twice per day	8
17	Greening et al. 2014	Intensity tolared	Symmetrical biphasic	50 Hz	QDC and NI	300 ms	15/5	30	Daily	6
18	Akinlabi et al. 2013	NI	NI	NI	NI	NI	NI	NI	2	8
19	Latimer et al. 2013	Maximal tolerated	NI	NI	NI	NI	NI	30	5	6
20	Vivodtzev et al. 2012	Maximal tolerated	NI	50 Hz	QDC/CM and NI	400 ms	6/16	35 min of QDC and 25 min of CM	5	6
21	Zanotti et al. 2012	20 up to 60 mA	Symmetrical biphasic	60–80 Hz	QDC and NI	NI	NI	30	5	5
22	DalĺAcqua et al. 2012	Maximal tolerated	Russian current	5 a 120 Hz	Rectus and oblique abdominal and NI	NI	4/1	25	Daily	NI
23	Giavedoni et al. 2012	Maximal tolerated	Asymmetrical Biphasic	50 Hz	QDC and NI	400 ms	8/20	30	Daily	2
24	Abdellaoui et al. 2011	Maximal tolerated	Biphasic symmetric	35 Hz	QDC/HM and NI	400 ms	NI	60	5	6
25	Nápolis et al. 2011	Maximal tolerated	Symmetrical Biphasic	50 Hz	QDC and NI	300 to 400 ms	2/10	NI	5	6
26	Dang et al. 2011	NI	NI	NI	NI	NI	NI	NI	NI	NI
27	Dal Corso et al. 2007	Initial intensity was set to create a visible contraction	Biphasic	50 Hz	QDC	400 ms	2/10 to 5/25 to 10/30 to 10/20	Week 1 = 15 minWeek 2 = 30 minWeek 3–6 = 1 h	5	6
28	Vivodtzev et al. 2006	Maximal tolerated.	Symmetrical Biphasic	35 Hz	QDC and electrode 8 × 4 cm and 4 × 4 cm	400 ms	7/8	>30	4	4
29	Gigliotti et al. 2004	NI	NI	NI	NI	NI	NI	NI	NI	NI
30	Zanotti et al. 2003	NI	Symmetrical Biphasic	8 Hz a 35 Hz	QDC plus vastus glutei and NI	250–350 ms	NI	30	5	4
31	Neder et al. 2002	Maximal tolerated	Symmetrical Biphasic	50 Hz	QDC and NI	300 to 400 ms	2/18 to 5/25 to 10/30	15 min in the first week and 30 min thereafter	5	6
32	Bourjeily-Habr et al. 2002	Visible contraction (range 55 to 120 mA)	NI	50 Hz	QDC/HM/CM and 2 electrodes (8 × 6 cm)	200 ms every 1500	NI	20	3	6

NI: not informed; QDC: quadriceps; HM: hamstring; CM: calf muscle; SMT: semitendinosus; SMM: semimembranosus; ICU: intensive care unit.

The parameters used in the application of neuromuscular electrical stimulation were reported in the studies and described the progressive nature of the programs. The duration of programs ranged from 2 to 24 weeks, and the length of the sessions was from 15 to 60 min. The frequency of sessions ranged from 2 to 7 times per week. The intensity of neuromuscular electrical stimulation in most trials was adjusted to obtain visible muscle contraction. Table 3 summarizes the neuromuscular electrical stimulation characteristics of the included studies.

Two studies compared neuromuscular electrical stimulation alone versus Sham and evaluated the exercise capacity by peak oxygen consumption as an outcome. One study performed the intervention in a rehabilitation center and other study in home-based environment. The meta-analyses showed (Figure 2) no significant improvement in peak oxygen consumption of 27.98 (95% CI: −71.41, 127.385, N = 22) was found for participants in the neuromuscular electrical stimulation group compared to sham group.

Six studies^{23,30–33,36} assessed exercise capacity as an outcome (neuromuscular electrical stimulation alone versus Sham), four of them used six-minute walk test^23,31–33 and two used endurance or incremental shuttle walking test^30,36 Due to the difference between the instruments used in the assessment of exercise capacity, we performed a meta-analysis with standardized mean difference. The meta-analyses showed that the exercise capacity was significantly higher among treated patients with neuromuscular electrical stimulation compared to patients in the sham group (1.10, 95% CI: 0.33, 1.86, N = 147) (Figure 3).

In this context, six studies^{23,30–33,36} assessed muscle strength as an outcome, three of them used an isokinetic dynamometer^31,33,36 and three used isometric maximum voluntary contraction^22,29,31 Four studies performed the intervention in a rehabilitation center and two studies in home-based environment. Due to the difference between the instruments used in the assessment of muscle strength, we performed a meta-analysis with standardized mean difference. The muscle strength (in newtons) was significantly higher among treated patients with neuromuscular electrical stimulation compared to patients in the sham group (0.53, 95% CI: 0.20, 0.87, N = 147) (Figure 4).

Additionally, seven studies^{22,25,26,34,35,41,50} combined neuromuscular electrical stimulation and conventional rehabilitation versus Conventional Rehabilitation and assessed six minutes walking test as an outcome. The meta-analyses showed (Figure 5) a significant improvement in 6MWT of 34.28 meters (95% CI: 6.84, 61.73, N = 262) for participants in the combined Neuromuscular electrical stimulation and conventional rehabilitation group compared to conventional rehabilitation group.

Three studies^25,26,35 assessed quality of life as an outcome (combined neuromuscular electrical stimulation and conventional rehabilitation versus Conventional Rehabilitation). The meta-analyses showed (Figure 6) no significant difference in quality of life total score of −2.46 (95% CI: −6.80, 1.89, N = 130) for participants in the combined neuromuscular electrical stimulation and conventional rehabilitation group compared to conventional rehabilitation group.

Discussion

The main results of our systematic review indicate that neuromuscular electrical stimulation significantly improve the exercise capacity and muscle strength in chronic obstructive pulmonary disease patients. However, the observed values for these two outcomes are below the minimal clinical important difference. These findings highlight that neuromuscular electrical stimulation improve, significantly, outcomes related to disabilities and activity limitation of individuals affected by chronic obstructive pulmonary disease, but without reaching the minimal clinical important difference for them.

Patients with COPD find exercise limitations and experience breathless. High quality evidence shows moderate to high effects for exercise programs (pulmonary rehabilitation) on health-related quality of life and exercise capacity in patients with COPD.⁵¹ In addition, pulmonary rehabilitation is effective in relieving dyspnea and fatigue, improving emotional function, and increasing their sense of control over health condition. However, for some COPD patients, exercising at a level high enough to improve their thigh muscles is difficult because they easily experience severe breathless with exercise. In these people, it may be that using an electrical current to stimulate the thigh muscles helps to improve this condition.⁵²

However, for some patients with chronic obstructive pulmonary disease, exercising at a level high enough to improve their thigh muscles is difficult because they easily experience severe breathless with exercise.⁵¹ In these people, it may be that using an electrical current to stimulate the thigh muscles helps to improve this condition.⁵¹

Therefore, neuromuscular electrical stimulation could be an adjunct treatment used to improve muscle strength and exercise capacity. Thus, neuromuscular electrical stimulation is a potential tool in the rehabilitation of aged and chronic diseases patients.^48,53 The strength of our study is the update of the previous systematic review^8–11 and the inclusion of the new studies that analyzed the effects of the neuromuscular electrical stimulation in chronic obstructive pulmonary disease patients. Moreover, the outcomes included considered in our analysis are related to prognosis in chronic obstructive pulmonary disease patients

Considering that six minutes walking test is also associated with ability to perform activities of daily living,⁵⁴ our meta-analysis showed a significant improvement in this variable of the 34.28 meters in the neuromuscular electrical stimulation combined to rehabilitation when compared to conventional rehabilitation alone. The minimal clinical important difference for the six minutes walking test in chronic obstructive pulmonary disease patients was estimated to be 25–80 meters.^55,56 However, it is important to note that the Holland et al. 2010⁵⁶ states that the minimal clinical important difference in patients with chronic obstructive pulmonary disease is conservatively 54 to 80 meters. Wise et al. 2005⁵⁴ gives a value of 25 meters, but also states that those patients who reported a “small change” improved by 60 meters, and those who reported a “substantial change” improved by 78 meters.

Thus, the mean difference observed between groups may be not considered substantial and contribute to the patient achieving the MCID Thus, the light of current knowledge, this data is not in favor to the recommendation of neuromuscular electrical stimulation, combined with conventional rehabilitation, in this population. Additionally, it is important to consider the cost of adding neuromuscular electric stimulation to a rehabilitation program for patients with chronic obstructive pulmonary disease. The same benefits have been observed for the use of electrostimulation alone (values below the minimal clinical important difference).

Additionally, the increased observed in muscle strength (neuromuscular electrical stimulation versus SHAM) was significantly but small, 0.53 N. Muscle function can be assessed using various methodologies and some are effort dependent (isometric, isokinetic, and isotonic testing) and others are not (nerve femoralis magnetic stimulation).⁵⁷

In this context, it is difficult to make a pragmatic recommendation about neuromuscular electrical stimulation in chronic obstructive pulmonary disease patients to muscle strength improvement.⁵⁸ The Official ATS/ERS statement on limb muscle dysfunction in chronic obstructive pulmonary disease.⁴ However there is no standardization of test procedures, it is difficult to draw conclusions about what increase in muscle function / mass really is clinically relevant. In the light of current knowledge, there is no clinically important minimal difference developed to assess the relevance of muscle function / mass increments.⁵⁹

Thus, caution is warranted when interpreting the present results given the differences in stimulation protocols used in the studies. The results of neuromuscular electrical stimulation depends on the capacity to evoke forces (moderate to high) for prolonged periods.⁶⁰ neuromuscular electrical stimulation could induce low muscle force and rapid muscle fatigue and limit the stimulus provided to the neuromuscular system and subsequent adaptations.⁶⁰ Researchers highlight that distributed neuromuscular electrical stimulation techniques, using multiple electrode pairs to stimulate the muscle or nerve, show promise in producing higher forces with less fatigue and discomfort than traditional (single-channel) neuromuscular electrical stimulation.⁶⁰ Thus, far problems in electrical stimulation protocols may have limitations to identify favorable results associated with electrical stimulation and further studies are required to elucidate this point.

Furthermore, was observed significant heterogeneity evident in the primary analyses. Most the included studies did not report concealment allocation or randomization in an appropriate way, which may have affected the results. It is not known whether the outcomes assessors were blinded in most studies and the outcomes in question are highly influential if the evaluator or the patient is aware of the intervention received. These issues generally limit the quality of evidence. Finally, the different protocols used to apply the neuromuscular electrical stimulation also may hinder the use of the intervention in clinical practice. Further research is required to investigate how to sustain positive effects of neuromuscular electrical stimulation over time and to determine essential attributes (mode, frequency, intensity, and duration).

From a clinical point of view, neuromuscular electrical stimulation improves exercise capacity compared to exercise alone and muscle strength compared to SHAM but, this improvement, is not enough to reach the MCID. Thus, our findings may be useful to help the decision-making of physiotherapists considering the cost of this intervention.

In order to improve the quality of evidence, future randomised controlled trials should have larger sample sizes and use appropriate methodological conduct of the study. In addition, to facilitate comparison of studies, efforts should be made to standardize the use of neuromuscular electrical stimulation protocol and make it available to the research and clinical community.

Considering the available data, our meta-analysis showed that neuromuscular electrical stimulation resulted in small improvement in exercise capacity and muscle strength in individuals affected by chronic obstructive pulmonary disease. Thus, the inclusion of neuromuscular electrical stimulation in rehabilitation programs must consider the cost Further larger and better RCTs are required to investigate the effects of neuromuscular electrical stimulation. It is important to highlight that most of the studies presented low methodological quality.

Clinical messages

Neuromuscular electrical stimulation promotes small improvement in exercise capacity and muscle strength of patients with chronic obstructive pulmonary disease.

The quality of the evidence is insufficient to conclude about the effectiveness of neuromuscular electrical stimulation.

Problems in electrical stimulation protocols may have limitations to identify favorable results.

Supplemental Material

sj-doc-1-cre-10.1177_02692155211067983 - Supplemental material for Effects of neuromuscular electrical stimulation on exercise capacity, muscle strength and quality of life in COPD patients: A Systematic Review with Meta-Analysis

Supplemental material, sj-doc-1-cre-10.1177_02692155211067983 for Effects of neuromuscular electrical stimulation on exercise capacity, muscle strength and quality of life in COPD patients: A Systematic Review with Meta-Analysis by Iura Gonzalez Nogueira Alves, Cássio Magalhães da Silva e Silva, Bruno Prata Martinez, Rodrigo Santos de Queiroz and Mansueto Gomes-Neto in Clinical Rehabilitation

Footnotes

Acknowledgements

None. Only the authors have contributed to the writing of this manuscript.

Author contributions

All the authors designed and conceptualized the study, collected and interpreted the data. The first draft of the manuscript was written by Iura Gonzalez N Alves and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship and/or publication of this article.

ORCID iDs

Iura Gonzalez Nogueira Alves

Cássio Magalhães da Silva e Silva

Mansueto Gomes-Neto

Supplemental material

Supplemental material for this article is available online.

References

Rodriguez-Roisin

Rabe

Vestbo

, et al. Global initiative for chronic obstructive lung disease (GOLD) 20th anniversary: a brief history of time. Eur Respir J 2017; 50: 1700671.

Gea

Casadevall

Pascual

, et al. Clinical management of chronic obstructive pulmonary disease patients with muscle dysfunction. J Thorac Dis 2016; 8: 3379–3400.

Barreiro

Gea

. Respiratory and limb muscle dysfunction in COPD. COPD 2015; 12: 413–426.

Maltais

Decramer

Casaburi

, et al. An official American thoracic society/european respiratory society statement: update on limb muscle dysfunction in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2014; 189: e15–e62.

Jones

Man

Gao

, et al. Neuromuscular electrical stimulation for muscle weakness in adults with advanced disease. Cochrane Database Syst Rev 2016; 10: CD009419.

Sillen

Franssen

Gosker

, et al. Metabolic and structural changes in lower-limb skeletal muscle following neuromuscular electrical stimulation: a systematic review. PLoS One 2013; 8: e69391.

Saitoh

Dos Santos

Anker

, et al. Neuromuscular electrical stimulation for muscle wasting in heart failure patients. Int J Cardiol 2016; 225: 200–205.

Sillen

MJH

Speksnijder

Eterman

, et al. Effects of neuromuscular electrical stimulation of muscles of ambulation in patients with chronic heart failure or COPD: a systematic review of the English-language literature. Chest 2009; 136: 44–61.

Chen

Guan

, et al. Effectiveness of neuromuscular electrical stimulation for the rehabilitation of moderate-to-severe COPD: a meta-analysis. Int J Chron Obstruct Pulmon Dis 2016; 11: 2965–2975. eCollection 2016.

10.

Pan

Guo

Liu

, et al. Lack of efficacy of neuromuscular electrical stimulation of the lower limbs in chronic obstructive pulmonary disease patients: a meta-analysis. Respirology 2014; 19: 22–29.

11.

Hill

Cavalheri

Mathur

, et al. Neuromuscular electrostimulation for adults with chronic obstructive pulmonary disease. Cochrane Database Syst Rev 2018; 5: CD010821.

12.

Moher

Liberati

Tetzlaff

, et al. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Br Med J 2009; 339: b2535.

13.

Higgins JPT, Thomas J, Chandler J, Cumpston M, Li T, Page MJ, Welch VA (editors). Cochrane Handbook for Systematic Reviews of Interventions version 6.2 (updated February 2021). Cochrane, 2021. Available from www.training.cochrane.org/handbook.

14.

Olivo

Macedo

Gadotti

, et al. Scales to assess the quality of randomized controlled trials: a systematic review. PhysTher 2008; 88: 156–175.

15.

Verhagen

de Vet

HCW

de Bie

, et al. The delphi list: a criteria list for quality assessment of randomized clinical trials for conducting systematic reviews developed by delphi consensus. J ClinEpidemiol 1998; 51: 1235–1241.

16.

Gomes-Neto

Rodrigues-

Jr Silva-

Jr , et al. Effects of yoga in patients with chronic heart failure: a meta-analysis. Arq Bras Cardiol 2014; 103: 433–439.

17.

Higgins

Thompson

Deeks

, et al. Measuring inconsistency in meta-analyses. Br Med J 2003; 327: 557–560.

18.

Collaboration TC. Available at: www.cochrane.org. [Accessed 3 may 2021].

19.

Bonnevie

Gravier

Debeaumont

, et al. Home-based neuromuscular electrical stimulation as an add-on to pulmonary rehabilitation does not provide further benefits in patients with chronic obstructive pulmonary disease: a multicenter randomized trial. Arch Phys Med Rehabil 2018; ;99(8):1462–1470. doi: 10.1016/j.apmr.2018.01.024.

20.

Medrinal

Prieur

Combret

, et al. Functional electrical stimulation-A new therapeutic approach to enhance exercise intensity in chronic obstructive pulmonary disease patients: a randomised controlled cross-over trial. Arch Phys Med Rehabil 2018; 99(8):1454–1461. doi: 10.1016/j.apmr.2018.02.002.

21.

Valenza

Torres-Sánchez

López-López

, et al. Effects of home-based superimposed neuromuscular electrical stimulation in severe chronic obstructive pulmonary disease patients: a randomized controlled clinical trial. Eur J Phys Rehabil Med 2017; 54(3):323–332. doi: 10.23736/S1973-9087.17.04745-1

22.

Kucio

Niesporek

Kucio

, et al. Evaluation of the effects of neuromuscular electrical stimulation of The lower limbs combined with pulmonary rehabilitation on exercise tolerance in patients with chronic obstructive pulmonary disease. J Hum Kinet 2016; 54: 75–82.

23.

Maddocks

Nolan

Man

, et al. Neuromuscular electrical stimulation to improve exercise capacity in patients with severe COPD: a randomised double-blind, placebo-controlled trial. Lancet Respir Med 2016; 4: 27–36.

24.

Akar

Günay

Sarinc Ulasli

, et al. Efficacy of neuromuscular electrical stimulation in patients with COPD followed in intensive care unit. Clin Respir J 2017; 11: 743–750.

25.

Tasdemir

Inal-Ince

Ergun

, et al. Neuromuscular electrical stimulation as an adjunct to endurance and resistance training during pulmonary rehabilitation in stable chronic obstructive pulmonary disease. Expert Rev Respir Med 2015; 9: 493–502.

26.

Vieira

Chiappa

Cipriano

, et al. Neuromuscular electrical stimulation improves clinical and physiological function in COPD patients. Respir Med 2014; 108: 609–620.

27.

Sillen

Franssen

Delbressine

, et al. Efficacy of lower-limb muscle training modalities in severely dyspnoeic individuals with COPD and quadriceps muscle weakness: results from the DICES trial. Thorax 2014; 69: 525–531.

28.

Greening

Williams

Hussain

, et al. An early rehabilitation intervention to enhance recovery during hospital admission for an exacerbation of chronic respiratory disease: randomised controlled trial. Br Med J 2014; 349: g4315.

29.

Dall’ Acqua

Dohnert

dos Santos

. Neuromuscular electrical stimulation with Russian current for expiratory muscle training in patients with chronic obstructive pulmonary disease. J Phys Ther Sci 2012; 24: 955–959.

30.

Vivodtzev

Debigaré

Gagnon

, et al. Functional and muscular effects of neuromuscular electrical stimulation in patients with severe COPD: a randomized clinical trial. Chest 2012; 141: 716–725.

31.

Nápolis

Dal Corso

Neder

, et al. Neuromuscular electrical stimulation improves exercise tolerance in chronic obstructive pulmonary disease patients with better preserved fat-free mass. Clinics (Sao Paulo) 2011; 66: 401–406.

32.

Abdellaoui

Préfaut

Gouzi

, et al. Skeletal muscle effects of electrostimulation after COPD exacerbation: a pilot study. Eur Respir J 2011; 38: 781–788.

33.

Dal Corso

Nápolis

Malaguti

, et al. Skeletal muscle structure and function in response to electrical stimulation in moderately impaired COPD patients. Respir Med 2007; 101: 1236–1243.

34.

Vivodtzev

Pépin

Vottero

, et al. Improvement in quadriceps strength and dyspnea in daily tasks after 1 month of electrical stimulation in severely deconditioned and malnourished COPD. Chest 2006; 129: 1540–1548.

35.

Zanotti

Felicetti

Maini

, et al. Peripheral muscle strength training in bed-bound patients with COPD receiving mechanical ventilation: effect of electrical stimulation. Chest 2003; 124: 292–296.

36.

Bourjeily-Habr

Rochester

Palermo

, et al. Randomised controlled trial of transcutaneous electrical muscle stimulation of the lower extremities in patients with chronic obstructive pulmonary disease. Thorax 2002; 57: 1045–1049.

37.

Neder

Sword

Ward

, et al. Home based neuromuscular electrical stimulation as a new rehabilitative strategy for severely disabled patients with chronic obstructive pulmonary disease (COPD). Thorax 2002; 57: 333–337.

38.

Péran

Castel

Beaumont

. Effets de l’électrostimulation neuromusculaire combinée des triceps suraux et des quadriceps dans la BPCO sévère et très sévère lors d’un programme de réhabilitation respiratoire. Kinesitherapie 2018; 18: 877–887.

39.

Zanotti

Bizzarri

Grasso

, et al. Combination of pulmonary rehabilitation and neuromuscular electrical stimulation in COPD patients: a randomized clinical trial of efficacy. J Pulmonar Respirat Med 2012; 2:1–6. doi:10.4172/2161-105X.1000112

40.

Giavedoni

Deans

McCaughey

, et al. Neuromuscular electrical stimulation prevents muscle function deterioration in exacerbated COPD: a pilot study. Resp Med 2012; 10: 1429–1434.

41.

Mekki

Paillard

Sahli

, et al. Effect of adding neuromuscular electrical stimulation training to pulmonary rehabilitation in patients with chronic obstructive pulmonary disease: randomized clinical trial. Clin Rehabil 2019; 33: 195–206.

42.

Gigliotti

Ballini

Bertolini

, et al. Effect of neuromuscular electrical stimulation (NMES) as an adjunct to an exercise training program (EXT) in patients with severe COPD. Eur Respir J 2004; 24: 256s.

43.

Dang

Gluck

Pirnay

, et al. Interest of neuromuscular electro-stimulation (NMES) in COPD patients during an ambulatory comprehensive respiratory rehabilitation program. Eur Respir J 2011; 38: p4807.

44.

Akinlabi

Main

Garrod

, et al. Neuromuscular electrical stimulation (NMES), A new strategy in the pulmonay rehabilitation of patients with severe and very severe MRC 4 and 5 chronic obstrutive pulmonary disease (COPD). Thorax 2013 68: A17. doi: 10.1136/thoraxjnl-2013-204457.35

45.

Latimer

Greening

Morgan

, et al. Unilateral neuromuscular electrical stimulation (NMES) of the quadriceps muscles in stable COPD. Eur Respir J 2013; 42: P3571.

46.

Dolmage

Brooks

Goldstein

. The effects Of high And Low frequency transcutaneous electrical muscle stimulation (tcems) On exercise In patients With COPD: a pilot study. ATS J 2016; 193: A3990.

47.

Tardif

Roy

Viacroze

, et al. Does neuromuscular electrical stimulation of the quadriceps during rehabilitation in COPD outpatients adds a benefit? Eur Respir J 2013; 46: OA1755.

48.

Chen

Jiang

, et al. Effect of transcutaneous neuromuscular electrical stimulation on prevention of intensive care unit-acquired weakness in chronic obstructive pulmonary disease patients with mechanical ventilation. Zhonghua Wei Zhong Bing Ji Jiu Yi Xue. 2019; 31: 709–713.

49.

Lopez Lopez

Granados Santiago

Donaire Galindo

, et al. Efficacy of combined electrostimulation in patients with acute exacerbation of COPD: randomised clinical trial. Med Clin (Barc) 2018; 151: 323–328. English, Spanish.

50.

Acheche

Mekki

Paillard

, et al. The effect of adding neuromuscular electrical stimulation with endurance and resistance training on exercise capacity and balance in patients with chronic obstructive pulmonary disease: a randomized controlled trial. Can Respir J 2020; 2020: 9826084. PMID: 33062081

51.

Puhan

Gimeno-Santos

Cates

, et al. Pulmonary rehabilitation following exacerbations of chronic obstructive pulmonary disease. Cochrane Database Syst Rev 2016; 12: CD005305. PMID: 27930803; PMCID: PMC6463852.

52.

McCarthy

Casey

Devane

, et al. Pulmonary rehabilitation for chronic obstructive pulmonary disease. Cochrane Database Syst Rev 2015; (2): CD003793. doi: 10.1002/14651858.CD003793.pub3. PMID: 25705944.

53.

Hong

Sui

Zhuang

, et al. Effectiveness of neuromuscular electrical stimulation on lower limbs of patients With hemiplegia after chronic stroke: a systematic review. Arch Phys Med Rehabil 2018; 99(5):1011–1022.e1. doi: 10.1016/j.apmr2017.12.019.

54.

American Thoracic Society, Board of Directors. ATS Statement: guidelines for the six-minute walk test Am J Respir Crit Care Med 2002; 166: 111–117.

55.

Wise

Brown

. Minimal clinically important differences in the six-minute walk test and the incremental shuttle walking test. COPD 2005; 2: 125–129.

56.

Holland

Hill

Rasekaba

, et al. Updating the minimal important difference for six-minute walk distance in patients with chronic obstructive pulmonary disease. Ach Phys Med Rehabil 2010; 91: 221–225.

57.

Marklund

Bui

Nyberg

. Measuring and monitoring skeletal muscle function in COPD: current perspectives. Int J Chron Obstruct Pulmon Dis 2019; 14: 1825–1838. PMID: 31695351; PMCID: PMC6707440.

58.

De Brandt

Spruit

Hansen

, et al. Changes in lower limb muscle function and muscle mass following exercise-based interventions in patients with chronic obstructive pulmonary disease: a review of the English-language literature. Chron Respir Dis 2018; 15: 182–219.

59.

Wouters

. Minimal clinically important diferences in COPD: body mass index and muscle strength. COPD 2005; 2: 149–155.

60.

Blazevich

Collins

Millet

, et al. Enhancing adaptations to neuromuscular electrical stimulation training interventions. Exerc Sport Sci Rev 2021; 49(4): 244–252.

Supplementary Material

Please find the following supplemental material available below.

For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.

For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.

0.00 MB

0.04 MB