Scholarly article on topic 'Cyclical electrical stimulation increases strength and improves activity after stroke: a systematic review'

Cyclical electrical stimulation increases strength and improves activity after stroke: a systematic review Academic research paper on "Medical engineering"

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{Stroke / "Electrical stimulation" / Strength / "Systematic review" / Meta-analysis / "Randomised controlled trial"}

Abstract of research paper on Medical engineering, author of scientific article — Lucas R Nascimento, Stella M Michaelsen, Louise Ada, Janaine C Polese, Luci F Teixeira-Salmela

Abstract Question: Does electrical stimulation increase strength after stroke and are any benefits maintained beyond the intervention period or carried over to activity? Design: Systematic review with meta-analysis of randomised or controlled trials. Participants: Adults who have had a stroke. Intervention: Cyclical electrical stimulation applied in order to increase muscle strength. Outcome measures: Strength measures had to be representative of maximum voluntary contraction and were obtained as continuous measures of force or torque, or ordinal measures such as manual muscle tests. Activity was measured using direct measures of performance that produced continuous or ordinal data, or with scales that produced ordinal data. Results: Sixteen trials representing 17 relevant comparisons were included in this systematic review. Effect sizes were calculated as standardised mean differences because various muscles were studied and different outcome measures were used. Overall, electrical stimulation increased strength by a standardised mean difference (SMD) of 0.47 (95% CI 0.26 to 0.68) and this effect was maintained beyond the intervention period (SMD 0.33, 95% CI 0.07 to 0.60). Electrical stimulation also improved activity (SMD 0.30, 95% CI 0.05 to 0.56) and this effect was also maintained beyond the intervention period (SMD 0.38, 95% CI 0.09 to 0.66). Conclusion: Cyclical electrical stimulation increases strength and improves activity after stroke. These benefits were maintained beyond the intervention period with a small-to-moderate effect size. The sustained effect on activity suggests that the benefits were incorporated into daily life. Review registration: PROSPERO (CRD42013003895). [Nascimento LR, Michaelsen SM, Ada L, Polese JC, Teixeira-Salmela LF (2014) Cyclical electrical stimulation increases strength and improves activity after stroke: a systematic review. Journal of Physiotherapy 60: 22–30]

Academic research paper on topic "Cyclical electrical stimulation increases strength and improves activity after stroke: a systematic review"

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Journal of Physiotherapy xxx (2014) xxx-xxx

Journal of

PHYSIOTHERAPY

journal homepage www.elsevier.com/locate/jphys

Research

Cyclical electrical stimulation increases strength and improves activity

after stroke: a systematic review

Lucas R Nascimentoa b, Stella M Michaelsenac, Louise Adaa, Janaine C Polesea b, Luci F Teixeira-Salmelab

a Discipline of Physiotherapy, The University of Sydney, Australia;b Discipline of Physiotherapy, Universidade Federal de Minas Gerais;c Discipline of Physiotherapy,

Universidade do Estado de Santa Catarina, Brazil

KEY WORDS

ABSTRACT

Stroke

Electrical stimulation Strength

Systematic review Meta-analysis Randomised controlled trial

Question: Does electrical stimulation increase strength after stroke and are any benefits maintained beyond the intervention period or carried over to activity? Design: Systematic review with meta-analysis of randomised or controlled trials. Participants: Adults who have had a stroke. Intervention: Cyclical electrical stimulation applied in order to increase muscle strength. Outcome measures: Strength measures had to be representative of maximum voluntary contraction and were obtained as continuous measures of force or torque, or ordinal measures such as manual muscle tests. Activity was measured using direct measures of performance that produced continuous or ordinal data, or with scales that produced ordinal data. Results: Sixteen trials representing 17 relevant comparisons were included in this systematic review. Effect sizes were calculated as standardised mean differences because various muscles were studied and different outcome measures were used. Overall, electrical stimulation increased strength by a standardised mean difference (SMD) of 0.47 (95% CI 0.26 to 0.68) and this effect was maintained beyond the intervention period (SMD 0.33, 95% CI 0.07 to 0.60). Electrical stimulation also improved activity (SMD 0.30,95% CI 0.05 to 0.56) and this effect was also maintained beyond the intervention period (SMD 0.38,95% CI 0.09 to 0.66). Conclusion: Cyclical electrical stimulation increases strength and improves activity after stroke. These benefits were maintained beyond the intervention period with a small-to-moderate effect size. The sustained effect on activity suggests that the benefits were incorporated into daily life. Review registration: PROSPERO (CRD42013003895). [Nascimento LR, Michaelsen SM, Ada L, Polese JC, Teixeira-Salmela LF (2014) Cyclical electrical stimulation increases strength and improves activity after stroke: a systematic review. Journal of Physiotherapy 60: XX-XX]

© 2014 Australian Physiotherapy Association. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/3.0/).

Introduction

Recent data indicates that 30.7 million people in the world have experienced and survived a stroke.1 After a stroke, the loss of ability to generate normal amounts of force is a major contributorto activity limitations and also contributes to participation restrictions.2,3 Consequently, there has been a move to implement strengthening interventions into rehabilitation after stroke. Strength training is commonly considered to be progressive resistance exercise, but any intervention that involves attempted repetitive effortful muscle contraction can result in increased motor unit activity and strength after stroke.4 For example, electrical stimulation may have the potential to improve strength after stroke by increasing the activation of motor units and/or the cross sectional area of a muscle, even when patients are unable to undertake interventions involving resistance exercises.5

According to de Kroon et al6 electrical stimulation can be broadly divided into two categories: functional electrical stimulation and cyclical electrical stimulation. In functional electrical stimulation, one or more muscles are electrically stimulated during the performance of an activity with the aim of improving that activity. In cyclical electrical stimulation, a muscle is repetitively electrically stimulated at near maximum contraction with the aim of strengthening that muscle. Given that these two categories of electrical stimulation have different purposes, as well as different methods of application, it is important to examine them separately. There have been two systematic reviews examining the efficacy of electrical stimulation at increasing strength after stroke. A Cochrane review7 reported an effect size of 1.0 (95% CI 0.5 to 1.6) on wrist extensor strength; this was based on one randomised trial8 of cyclical electrical stimulation to the wrist and finger extensors versus no intervention. A second review5 reported a modest beneficial effect

http://dx.doi.org/10.1016/jjphys.2013.12.002

1836-9553/© 2014 Australian Physiotherapy Association. Published by Elsevier B.V. This is an open access article underthe CC BY-NC-ND license (http://creativecommons.org/ licenses/by-nc-nd/3.0/).

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on strength based on 11 trials of both functional and cyclical electrical stimulation versus no intervention or any other intervention. However, a meta-analysis was not performed due to statistical heterogeneity. Furthermore, both reviews are now over five years old. In addition, there has been no examination of the efficacy of electrical stimulation compared with other strengthening interventions or the efficacy of different doses or modes of electrical stimulation.

Therefore, the aim of this systematic review was to examine the efficacy of cyclical electrical stimulation (from now on referred to as electrical stimulation). The specific research questions were:

1. Does electrical stimulation increase strength after stroke? Are any benefits maintained beyond the intervention period or carried over to activity?

2. What is the effect of electrical stimulation on strength after stroke compared to each other type of strengthening intervention?

3. What is the effect of different doses or modes of electrical stimulation on strength after stroke?

In order to make recommendations based on a high level of evidence, this review included only randomised or controlled trials. Subgroup analyses based on time after stroke and initial level of strength were planned.

Method

Identification and selection of trials

Searches were conducted in MEDLINE (1946 to December 2012), CINAHL (1986 to December 2012), EMBASE (1980 to December 2012) and PEDro (to December 2012) for relevant studies without date or language restrictions. Search terms included: words related to stroke; words related to randomised, quasi-randomised or controlled trials; and words related to electrical stimulation (such as electric stimulation, neuromuscular stimulation, nerve stimulation and functional stimulation) (see Appendix 1 on the eAddenda for the full search strategy). Title and abstracts were displayed and screened by two reviewers in order to identify relevant studies. Full text copies of peer-reviewed relevant papers were retrieved and their reference lists were screened to identify further relevant studies. The method section of the retrieved papers was extracted and reviewed independently by two reviewers using predetermined criteria (Box 1). Both reviewers were blinded to authors, journals and results. Disagreement or ambiguities were resolved by consensus after discussion with a third reviewer.

Assessment of characteristics of trials

Quality

The quality of the included trials was assessed by extracting PEDro scores from the Physiotherapy Evidence Database26. The PEDro scale is a 11-item scale designed for rating the methodological quality (internal validity and statistical information) of randomised trials. Each item, except for Item 1, contributes one point to the total PEDro score (range: 0-10 points). Where a trial was not included in the database, it was scored by a reviewer who had completed the PEDro Scale training tutorial.

Participants

Trials involving adult participants of either gender at any time following stroke were included. The number of participants, age and time since stroke were recorded in order to describe the trials. Participants who were unable to move a limb through full range of movement against gravity were categorised as very weak; participants who could move through full range against gravity, but

Box 1. Inclusion criteria.

Design

• Randomised or controlled trial Participants

• Adults (>18 years old)

• Diagnosis of stroke

• Muscle weakness (Manual Muscle Test< Grade 4) Intervention

• Electrical stimulation in order to increase strength (ie, it is clearly stated that the aim of the intervention is to increase strength or strength is an outcome measure)

Outcomes measures

• Strength measured as peak force/torque and congruent with the stimulated muscle/s

Comparisons

• Electrical stimulation versus placebo/nothing or non-strengthening intervention

• Electrical stimulation versus any other strengthening intervention

• Electrical stimulation versus different dose/mode of electrical stimulation

had less than normal strength, were categorised as weak. At admission to the trial, participants who were less than six months after stroke were categorised as sub-acute and those who were more than six months after stroke were categorised as chronic.

Intervention

The experimental intervention was electrical stimulation that produced strong repetitive muscle contractions applied in order to increase muscle strength. The control intervention was defined according to each research question: (1) to examine the efficacy of electrical stimulation, the control intervention could be nothing, placebo or any other non-strengthening intervention; (2) to examine the effect of electrical stimulation compared with other strengthening interventions, the control intervention could be any other type of strengthening intervention; (3) to compare different doses or modes of electrical stimulation, the control intervention could be any other dose or mode.

Measures

The strength measurement had to be reported as peak force/torque generation and representative of maximum voluntary contraction (eg, manual muscle test or dynamometry). When multiple measures of strength were reported, the measure that reflected the trained muscle/s was used. If it was appropriate to use the measures from several different muscles (ie, these muscles had been targeted in the intervention), the means and SD of the individual measurements were summed.4 For measurement of activity, direct measures of performance were used regardless of whether they produced continuous data (eg, The Box and Block Test) or ordinal data (eg, Action Research Arm Test). Measures of general activity (eg, Barthel Index) were used if they were the only available measure of activity.

Data analysis

Information about the method (ie, design, participants, intervention and measures) and results (ie, number of participants, mean and SD of strength and activity) were extracted by two reviewers and checked by a third reviewer. Where information was not available in the published trials, details were requested from the corresponding author.

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Research

Since more trials reported pre-intervention and postintervention scores than change scores, post-intervention scores were used to obtain the pooled estimate of the effect of intervention immediately (ie, post intervention) and long-term (ie, after a period of no intervention). Sub-group analyses were performed for the primary outcome (ie, strength measure) according to the time after stroke (sub-acute, chronic), and the initial level of strength (very weak, weak). If only the median and range of outcomes were available, additional data were requested from the author. The effect size was reported as Cohen's standardised mean difference (95% CI), because different outcome measures were used. A fixed-effects model was used. In the case of significant statistical heterogeneity (I2 >50%), a random effects model was applied to check the robustness of the results. Post-hoc sensitivity analysis was performed if there was significant statistical heterogeneity. The analyses were performed using The MIX-Meta-Analysis Made Easy program27 Version 1.7.9,10 Where data were not available to be included in the pooled analysis, the between-group result was

reported. For all outcome measures, the critical value for rejecting H0 was set at a level of 0.05 (2-tailed).

Results

Flow of trials through the review

The electronic search strategy identified 6796 papers (excluding duplicates). After screening titles, abstracts and reference lists, 64 potentially relevant full papers were retrieved. Forty-eight papers failed to meet the inclusion criteria; therefore 16 papers were included in this systematic review. One of the papers reported a trial with three arms (cyclical electrical stimulation group, no-intervention group and alternative strengthening intervention group). Therefore, 17 relevant comparisons were reported among the 16 included trials. Figure 1 presents the flow of papers

Titles and abstracts screened (n = 8056)

• from MEDLINE (n = 4794) . from CINAHL (n = 540)

• from EMBASE (n = 2490)

• from PEDro (n = 232)

Duplicate papers between

databases (n = 1260)

Papers excluded after screening

titles/abstracts (n = 6734)

Potentially relevant papers retrieved for evaluation of full text (n = 64)

• from electronic databases (n = 62)

• from reference lists (n = 2)

Papers excluded after evaluation of full

text (n = 48)a

• study design not RCT or CT (n = 8)

• aim of experimental intervention is not

strengthening (n = 41)

• strength measure is not peak/torque

w generation (n = 5)

• control intervention is not related to

the research questions (n = 5)

• paper not available (n = 1)

• duplicate data (n = 1)

Papers included in systematic review (n = 16) Comparisons included in systematic review (n = 17)

Figure 1. Flow of studies through the review. aPapers may have been excluded for failing to meet more than one inclusion criterion.

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through the review. See Appendix 2 on the eAddenda for a summary of the excluded papers.

Characteristics of included trials

The 16 trials involved 638 participants and investigated the efficacy of electrical stimulation for increasing muscle strength after stroke. Details of the individual trials are presented in Table 1. Thirteen trials compared electrical stimulation with nothing/placebo, providing data to answer the first study question.8,11-22 Three trials compared electrical stimulation with other strengthening interventions, providing data to answer the second study question.16,23,24 One trial25 compared different doses/modes of electrical stimulation (ie, the third study question). Additional information was obtained from the authors for four papers.8,11,18,21

Quality

The mean PEDro score of the papers was 5 (range 2 to 7) (Table 2). The majority of trials: randomly allocated participants (88%); had similar groups at baseline (75%); had blinded assessors (56%); reported loss to follow-up of 15% or less (69%); reported between-group differences (81%); and reported point estimate and variability (94%). However, the majority of trials did not report that they concealed allocation (81%) or carried out an intention-to-treat analysis (88%). All trials, except one, did not blind therapists and participants, which is difficult for this intervention involving near maximum muscle contraction.

Participants

The mean age of participants ranged from 52 to 75 years old. In the trials of sub-acute participants, the mean time after stroke ranged from 1 week to 6 months (nine trials), whereas in trials of chronic participants it ranged from 2 to 5 years (seven trials) including additional information from the authors for two trials.11,18 Ten trials included very weak participants and six trials included weak participants.

Intervention

The experimental intervention was electrical stimulation (ten trials), position-triggered electrical stimulation (one trial), EMG-triggered electrical stimulation (three trials), and a combination of EMG-triggered or position-triggered electrical stimulation and electrical stimulation (two trials). Ten trials delivered usual therapy to both experimental and control groups. Fourteen trials applied electrical stimulation to one or two muscles per limb with only two trials13,22 applying it to four different muscles.

Outcome measures

Measures of strength were mainly maximum voluntary force production, either continuous measures of force or torque (14 trials), or ordinal measures such as manual muscle tests (two trials). Most trials used direct measures of activity (five trials reported continuous data, and three trials reported ordinal data), and only one trial used an indirect measure. Seven trials did not measure activity.

Effect of electrical stimulation

Strength

The overall effect of electrical stimulation on strength immediately after intervention was examined by pooling post-intervention data from 11 trials with a mean PEDro score of 5.1, representing moderate quality (Figure 2a, see Figure 3a on the eAddenda for the detailed forest plot). Overall, the effect size was 0.47 (95% CI 0.26 to 0.68) in favour of electrical stimulation. Two trials,8,12 that were unable to be included in the pooled analysis, also reported significant between-group differences in strength in favour of electrical

a Bakhtiary Heckmann Hui-Chan Kobayashi |-Kraft Mano

Rosewilliam Shin

Winchester Yan (2005) Yan (2009)

-2-10 1 2 favours con favours exp

Hui-Chan Kraft

Rosewilliam Yan (2005) Yan (2009)

favours con

01 favours exp

Figure 2. (a) Standardised mean difference (95% CI) of effect of electrical stimulation versus nothing/placebo on strength immediately after intervention (n=359). (b) Standardised mean difference (95% CI) of effect of electrical stimulation versus nothing/placebo on strength beyond the intervention period (n = 211).

stimulation. Maintenance of the benefit was examined by pooling post intervention data from five trials that measured strength beyond the intervention period. Overall, the increase in strength was maintained with an effect size of 0.33 (95% CI 0.07 to 0.60) (Figure 2b, see Figure 3b on the eAddenda for the detailed forest plot).

When the trials were grouped according to the initial level of strength, electrical stimulation increased the strength in very weak participants (eight trials) with an effect size of 0.40 (95% CI 0.17 to 0.65), and in weak participants (three trials) with an effect size of 0.66 (95% CI 0.21 to 1.11). When the trials were grouped according to the time after stroke, electrical stimulation increased the strength in sub-acute participants (six trials) with an effect size of 0.55 (95% CI 0.28 to 0.81), while in chronic participants (five trials) the effect size was 0.33 (95% CI -0.02 to 0.69).

Activity

The overall effect of electrical stimulation on activity immediately after intervention was examined by pooling post intervention data from six trials with a mean PEDro score of 5.7 out of 10 (Figure 4a, see Figure 5a on the eAddenda for the detailed forest plot). Overall, electrical stimulation improved activity with an effect size of 0.30 (95% CI 0.05 to 0.56). Of the two trials unable to be included in the pooled analysis, one trial16 reported that most of the participants were not able to perform the activity tests, and one trial8 reported a significant between-group effect on activity in

Table 1

Characteristics of included papers (n= 16).

Design

Participants

Intervention-1

Bakhtiary" RCT n = 40

Age (yr) = mean 55. range 42 to 65 Time since stroke (mo) = not reported Weakness = very weak

Bowman12 RCT n = 30

Age (yr) = not reported

Time since stroke (mo) = range 0.7 to 4.0

Weakness» weak

deKroon6-25 RCT n = 22

Age (yr) = mean 59. SD9

Time since stroke (mo) = mean 22. range 6 to 115 Weakness» weak

Heckmann" RCT n = 28

Age (yr) = 52, SD 23

Time since stroke (mo) = mean 2. SD 0.1 Weakness = very weak

Exp = ES

9 min 5/wk 4wk Con = nothing

Both = usual therapy (Bobath)

Exp = position-triggered ES 100 contractions 5/wk 4wk Con = nothing Both = usual therapy

Exp = ES

30 min 5/wk 6wk Con = EMG-triggered ES 30 min 5/wk 6wk

Exp = EMG-triggered ES 15 contractions 5/wk 4wk Con = nothing

Both = usual therapy (Bobath)

Hui-Chan14 RCT n=109

Age (yr) = mean 57, SD 8

Time since stroke (mo) = mean 56. SD 41

Weakness» weak

Exp = ES

60 min 5/wk 4wk Con = nothing

Kimberley2

Kobayashi15

Kraft16

Lima24

Mano17

Cross-over RCT

Age (yr) = mean 60. SD15

Time since stroke (mo) = mean 35. SD 25

Weakness = very weak

n = 24

Age (yr) = mean 64. SD11 Time since stroke (mo) = mean 31 Weakness = very weak

n = 22

Age (yr) = mean 63. SD 9

Time since stroke (mo) = mean 26. SD 13

Weakness» weak

Age (yr) = not reported

Time since stroke (mo) = not reported

Weakness» weak

Age (yr) = mean 74, SD 7

Time since stroke (mo) = mean 6, SD 3

Weakness = very weak

Exp = EMG-triggered ES + ES 6h 3.3/wk 3wk Con »voluntary effort + nothing 6h 3.3/wk 3wk

Exp = ES

30min 5/wk 6wk Con = nothing Both = usual therapy

Exp = EMG-triggered ES 60min 3/wk 12wk Con 1 = nothing Con 2 = strengthening (PNF) 60min 3/wk 12wk

Exp = ES

15min 10 sessions

Con »strengthening (isotonic)

3 15 reps 10 sessions

Exp = ES

30min 3/wk 8wk Con = nothing Both = usual therapy

Electrical stimulation

Outcome measures-1

Muscles = ankle dorsiflexors Frequency = 100 Hz Duration» 4s Progression» | intensity

Muscles =wrist extensors Frequency=35 Hz Duration» 8 s

Progression» | number of contractions

Muscles = wrist and finger extensors Frequency=35 Hz Duration» 6s Progression» | threshold

Muscles = elbow and wrist extensors, knee flexors, ankle plantarflexors Frequency = 80 Hz Duration» 1 s Progression» | threshold

Muscles = ankle dorsiflexors and plantarflexors Frequency = 100 Hz Duration»not reported Progression = not reported

Muscles = wrist and finger extensors Frequency = 20 Hz Duration» 5 s Progression = not reported

Muscles »shoulder abductors Frequency = 20 Hz Duration» 10s Progression = not reported

Muscles =wrist extensors Frequency=30 to 90 Hz Duration» 10s Progression» | threshold

Muscles = knee extensors Frequency = 50 Hz Duration» 10s Progression = not reported

Muscles = wrist and finger extensors Frequency = 50 Hz Duration» 5 s

Progression» | number of contractions

Strength = MMT (0 to 5); Ankle DF

Activity» not measured Timing: 0,4 wk

Strength = dynamometry (Nm); wrist Ext Activity» not measured Timing: 0,4 wk

Strength = dynamometry (Kg); grip strength Activity» ARAT (0 to 57) Timing: 0,4, 6,12 wk

Strength = MMT (0 to 5); E wrist Ext and ankle PF Activity» Barthel index Timing: 0,4 wk

Strength = dynamometry (JVm); E ankle DF and PF Activity = TUG (s) Timing: 0,4, 8 wk

Strength = dynamometry (JV); finger Ext Activity» BBT(# blocks) Timing: 0,3 wk

Strength = dynamometry (JV); shoulder abd Activity» not measured Timing: 0,6 wk

Strength = dynamometry (lb): grip strength Activity=JTHFT (s) Timing = 0, 12, 24, 48

Strength = dynamometry (Nm/s); knee Ext Activity» not measured Timing: 0,10 sessions

Strength »dynamometry (Kg); grip strength Activity» not measured Timing: 0, 8 wk

О) rD

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2. i 0 c

Table 1 (Continued)

Design

Participants

Intervention

Electrical stimulation

Outcome measures3

■a sr

isi ¡2 О

Powell8

Rosewilliam18

Shin19

Winchester20

Yan (2005)2

Yan (2009)2

n = 60

Age (yr) = mean 68, SD12

Time since stroke (mo) = mean 0.8, SD 0.2

Weakness = very weak

n = 90

Age (yr) = mean 75, SD11

Time since stroke (mo) = not reported

Weakness = very weak

Age (yr) = mean 58, SD 10

Time since stroke (mo)=mean 19, SD 6

Weakness = weak

n = 40

Age (yr) = mean 58, SD 12

Time since stroke (mo)=mean 2, SD 1

Weakness = very weak

n = 46

Age (yr) = mean 71, SD 8

Time since stroke (mo) = mean 0.3, SD 0.1

Weakness = very weak

n = 62

Age (yr) = mean 70, SD7

Time since stroke (mo) = mean 0.3, SD 0.1

Weakness = very weak

Exp = ES

90 min x 5/wk x 8wk Con = nothing Both = usual therapy

Exp = ES

60 min x 5/wk x 6wk Con = nothing Both = usual therapy

Exp = EMG-triggered ES 30 min x 5/wk x 10wk Con = nothing

Exp = Positional-triggered ES + ES 30 min x 5/wk x 4 wk + 2hr x 5/wk x 4wk Con = nothing Both = usual therapy

Exp = ES

30 min x 5/wk x 3wk Con = Sham stimulation 30 min x 5/wk x 3wk Both = usual therapy

Exp = ES

60 min x 5/wk x 3 wk Con = nothing Both = usual therapy

Muscles = wrist and finger extensors Frequency = 20 Hz Duration = 5 s

Progression = f number of contractions

Muscles = wrist and finger extensors Frequency = 40 Hz Duration = 3 s Progression = f intensity

Muscles = wrist and finger extensors Frequency=35 Hz Duration = 5 s Progression = f threshold

Muscles = knee extensors Frequency=30 Hz Duration = 10 s

Progression = f number and duration of contractions

Muscles = knee flexors and extensors, ankle dorsiflexors and plantarflexors Frequency=30 Hz Duration = not reported Progression = not reported

Muscles = ankle dorsiflexors and plantarflexors Frequency = 100 Hz Duration = not reported Progression = not reported

Strength = dynamometry (Nm) (15 deg); wrist Ext Activity = ARAT (0 to 57) Timing: 0, 8, 20,32wk

Strength = dynamometry (N); wrist Ext Activity = ARAT (0 to 57) Timing: 0,6,12, 24,36wk

Strength = dynamometry, (Kg); wrist Ext Activity=BBT(# blocks) Timing: 0, 10 wk

Strength = dynamometry (Nm); knee Ext Activity = not measured Timing: 0,4 wk

Strength = dynamometry (Nm); ankle DF Activity=TUG (s) Timing: 0,3, 8 wk

Strength = dynamometry (Nm); ankle DF Activity=TUG (s) Timing: 0, 3, 8 wk

su 3 D.

ARAT, action research arm test; abd, abduction; BBT, box and block test; Con, control group; CT, controlled trial; DF, dorsiflexion; Exp, experimental group; ES, electrical stimulation; Ext, extension; JTHFT, Jebsen-Taylor hand function test; MAL, motor activity log; MMT, manual muscle test; MVC, maximum voluntary contraction; PF, plantarflexion; PNF, proprioceptive neuromuscular facilitation; RCT, randomised clinical trial; TUG, Timed Up and Go test; S, summed.

a Groups and outcome measures listed are those that were analysed in this systematic review; there may have been other groups or measures in the paper.

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Table 2

PEDro criteria and scores for included papers (n = 16).

Study Random Concealed Groups Participant Therapist Assessor <15% Intention- Between-group Point estimate Total

allocation allocation similar at baseline blinding blinding blinding dropouts to-treat analysis difference reported and variability reported (0 to 10)

Bakhtiary11 Y N Y N N Y Y N Y Y 6

Bowman12 Y N N N N Y N N Y N 3

de Kroon6 25 Y Y N N N Y Y N Y Y 6

Heckmann13 Y N Y N N N Y N Y Y 5

Hui-Chan14 Y N Y N N Y Y Y Y Y 7

Kimberley23 Y N Y Y N Y Y N N Y 6

Kobayashi15 Y N N N N N Y N N Y 3

Kraft16 N N Y N N N Y N Y Y 4

Lima24 N N N N N N Y N N Y 2

Mano17 Y N Y N N N Y N Y Y 5

Powell8 Y Y Y N N Y Y N Y Y 7

Rosewilliam18 Y Y Y N N Y N Y Y Y 7

Shin19 Y N Y N N N N N Y Y 4

Winchester20 Y N Y N N N N N Y Y 4

Yan (2005)22 Y N Y N N Y Y N Y Y 6

Yan (2009)21 Y N Y N N Y N N Y Y 5

Y=yes, N = no.

a Heckmann Hui-Chan Rosewilliam Shin

Yan (2005) Yan (2009)

-3-2-10123 favours con favours exp

b Hui-Chan Rosewilliam Yan (2005) Yan (2009)

-3-2-10123 favours con favours exp

Figure 4. (a) Standardised mean difference (95% CI) of effect of electrical stimulation versus nothing/placebo on activity immediately after intervention (n = 242). (b) Standardised mean difference (95% CI) of effect of electrical stimulation versus nothing/placebo on activity beyond the intervention period (n= 198).

favour of the electrical stimulation group. Maintenance of the benefit was examined by pooling data from the four trials that reported results beyond the intervention period. A significant improvement in activity was maintained with an overall effect size of 0.38 (95% CI 0.09 to 0.66) (Figure 4b, see Figure 5b on the eAddenda for the detailed forest plot).

Effect of electrical stimulation on strength compared with other strengthening interventions

The effect of electrical stimulation compared with other strengthening interventions was examined by three trials, with a mean PEDro score of 4 out of 10. The alternative strengthening

interventions were maximum voluntary effort,23 external resistance applied during proprioceptive neuromuscular facilitation,16 or isotonic exercises.24 Although two trials16,23 reported no significant difference between electrical stimulation and another strengthening intervention, a meta-analysis was not possible because only one trial23 reported post-intervention data. The mean difference between groups in this trial was 4 N (95% CI -2.0 to 10.0). A third trial24 did not report a between-group statistical comparison.

Effect of different dose/mode of electrical stimulation on strength

One trial,25 with a PEDro score of 6 out of 10, compared the effect of electrical stimulation with EMG-triggered electrical stimulation. There was no significant difference in the ratio of paretic/non-paretic strength between the groups (MD 0.04, 95% CI -0.04 to 0.12).

Discussion

This systematic review provides evidence that electrical stimulation can increase strength and improve activity after stroke, and that benefits are maintained beyond the intervention period. However, the evidence about whether electrical stimulation is more beneficial than another strengthening intervention is sparse, and the relative effect of different doses or modes is still uncertain.

This systematic review set out to answer three questions. The first examined whether electrical stimulation increases strength and improves activity after stroke. The meta-analyses show that the implementation of electrical stimulation has a moderate positive effect on strength, which is accompanied by a small-to-moderate positive effect on activity. The slightly smaller effect on activity may be because only one trial22 applied electrical stimulation to more than two muscles per limb. This is unlikely to have a large impact on activities performed by that limb, because most activities require contraction of many muscles at one time or another. The improvements in strength and activity were maintained beyond the intervention period with a small-to-moderate effect size, suggesting that the benefits were incorporated into daily life. Furthermore, meta-analyses of the subgroups suggest that electrical stimulation can be applied effectively to both weak

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Nascimento et al: Electrical stimulation after stroke

and very weak people after stroke, subacutely, and may be applied chronically.

Two previous systematic reviews5,7 concluded that electrical stimulation was beneficial in increasing muscle strength after stroke. However, these conclusions were based on few trials, no meta-analysis and included trials of both cyclical and functional electrical stimulation. The results of the current systematic review provide stronger evidence of the efficacy of electrical stimulation for increasing strength and improving activity; this is because the conclusions are based on a meta-analysis of nine randomised trials and two controlled trials of reasonable quality. In addition, the trials included in the meta-analysis were similar with regard to the stimulation parameters (frequency and duration of the stimulus) and the amount of intervention delivered. Although the length of the individual sessions varied (mean 45 min per muscle, SD 38), the trials were very similar in their frequency (mean 4.6/wk, SD 0.7) and duration (mean 5.8 wk, SD 3.0) of intervention. The evidence appears strong enough to recommend that daily sessions of electrical stimulation with high repetitions of maximum muscle contractions be used to increase strength after stroke.

The second question examined whether electrical stimulation is more effective than other strengthening interventions for increasing strength after stroke. There are insufficient data to determine whether electrical stimulation is better than another strengthening intervention. Only three trials investigating this question were included and a meta-analysis could not be performed. Furthermore, the mean PEDro score of 4.0 from the three trials related to this question represents low quality, with considerable performance, attrition and detection bias present.

The third question examined the most effective dose or mode of electrical stimulation for increasing strength after stroke. There are insufficient data to provide evidence regarding the effect of different doses/modes of electrical stimulation. Only one trial25 directly compared two different modes and found no difference between electrical stimulation and EMG-triggered electrical stimulation, with an effect size near zero.

This review has both strengths and limitations. The mean PEDro score of 5.0 for the 16 trials included in this review represents moderate quality. A source of bias in the included trials was lack of blinding of therapists and participants, since it is very difficult to blind therapists or participants during the delivery of complex interventions. Other sources of bias were lack of reporting concealed allocation or whether an intention-to-treat analysis was undertaken. On the other hand, the main strength of this review is that only trials where electrical stimulation was applied in order to increase strength and with a clear measure of force generation were included; this makes the results specific to the research questions. Additionally, publication bias inherent to systematic reviews was avoided by including studies published in languages otherthan

English.17,24

In conclusion, this systematic review provides evidence that cyclical electrical stimulation is effective (ie, it results in a greater increase in muscle strength compared with placebo/nothing). Electrical stimulation appears to be effective regardless of the initial level of strength or the time after stroke and the benefits are maintained beyond the intervention period. Clinicians should therefore be confident in prescribing daily electrical stimulation for people after a stroke, when the primary objective of the intervention is to increase muscle strength. In particular, it may be a useful intervention in the presence of cognitive impairments or profound weakness when it is difficult for the person to carry out strengthening exercises independently. In addition, the results of this systematic review are valuable since they show that electrical stimulation can have a beneficial effect not only on strength but also on activity, with improvements maintained beyond the

intervention period. Further studies are necessary to investigate whether electrical stimulation is more effective than other strengthening interventions.

What is already known on this topic: After a stroke, many people are unableto generate normal amounts of force, which restricts participation in daily activities. Cyclical electrical stimulation can be used to strengthen muscles, even when the patient cannot voluntarily generate adequate force for resistance exercise.

What this study adds: Cyclical electrical stimulation increases strength and activity in people who have had a stroke. These effects are maintained beyond the intervention period, suggesting that the increased strength is utilised in daily life and is therefore maintained by ongoing increased activity.

eAddenda: Figures 3a, 3b, 5a, 5b and Appendix 1 and 2 can be found online at doi:10.1016/j.jphys.2013.12.002 Competing interests: Nil.

Acknowledgements: Brazilian Government Funding Agencies (CAPES, CNPq, and FAPEMIG) for the financial support.

Correspondence: Louise Ada, Discipline of Physiotherapy, Faculty of Health Sciences, The University of Sydney, Australia. Email: louise.ada@sydney.edu.au

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