Does Sensory Transcutaneous Electrical Stimulation Enhance Motor Recovery Following a Stroke? A Systematic Review

Abstract

Background. Somatosensory input may lead to long-lasting cortical plasticity enhanced by motor recovery in patients with neurological impairments. Sensory transcutaneous electrical stimulation (TENS) is a relatively risk-free and easy-to-implement modality for rehabilitation. Objective. The authors systematically examine the effects of sensory TENS on motor recovery after stroke. Methods. Eligible randomized or quasi-randomized trials were identified via searches of computerized databases. Two assessors reviewed independently the eligibility and methodological quality of the retrieved articles. Results. In all, 15 articles satisfied the inclusion criteria. Methodological quality was generally good, with a mean (standard deviation) PEDro score of 6.7/10 (1.2). Although the majority of studies reported significant effects on at least 1 outcome measure, effect sizes were generally small. Meta-analysis could not be performed for the majority of outcome measures because of variability between studies and insufficient data. A moderate effect was determined for force production of the ankle dorsiflexors and for the Timed Up and Go test. Conclusions. Sensory stimulation via TENS may be beneficial to enhance aspects of motor recovery following a stroke, particularly when used in combination with active training. Because of the great variability between studies, particularly in terms of the timing of the intervention after the stroke, the outcome measures used, and the stimulation protocols, insufficient data are available to provide guidelines about strategies and efficacy.

Keywords

sensory transcutaneous electrical stimulation stroke rehabilitation motor recovery somatosensory

Introduction

Sensory input is required for maintaining normal cortical representations within the sensory and motor cortex, and motor performance as well as motor skills acquisition are dependent on somatosensory input.^1-3 Not surprisingly, somatosensory deficits following a brain insult, such as a stroke, are associated with slower recovery of motor function.^4,5 Research evidence from both animals and humans with no cortical impairments indicates that somatosensory inputs can induce plastic changes in the brain as they effect corticomotor excitability of the areas representing the stimulated body part that may outlast the stimulation period.^6-11 It has therefore been postulated that augmenting somatosensory input may lead to long-term plasticity and enhanced motor recovery in patients with neurological impairments.^3,12

Various modes of somatosensory input have been used as therapeutic interventions to enhance motor recovery following stroke, including needle electroacupuncture,¹³ repetitive passive movement,¹⁴ and mechanical vibration.¹⁵ Transcutaneous electrical stimulation (TENS) is an additional modality that can provide sensory input by peripheral nerve stimulation via electrodes placed on the skin. Adjustment of the stimulation intensity, which is achieved primarily by manipulating pulse duration, pulse frequency, and/or current amplitude, determines whether the evoked responses are merely sensory or also include muscle contractions.¹⁶

Although sensory TENS is frequently used in rehabilitation, primarily for pain modulation,^17,18 there has been a growing interest in the past decade in its use as a means of enhancing motor recovery following a stroke.^3,12 TENS stimulators are readily available, relatively cheap, and risk free, and unlike needle electroacupuncture, can be easily applied and controlled by most individuals, particularly if the stimulation remains at a pleasant sensory level.¹⁶ Should it be found that somatosensory input via TENS can enhance motor recovery following a stroke, this noninvasive modality could be easily incorporated as part of the rehabilitation treatment regimen. Thus, the purpose of the present review is to determine the therapeutic effect that sensory TENS has on motor recovery following a stroke.

Methods

Literature Search Methods

A computerized search of articles published in English was conducted independently by the 2 authors. The following databases were searched from their inception to January 2010: PubMed, EMBASE, CINHAL, ISI Science Citation Index, Cochrane library, Cochrane Stroke Group Trials Register, Hooked on Evidence, and the Physiotherapy Evidence Database (PEDro). Articles appearing in these databases ahead of publication were also included. Reference sections of relevant review and research articles were used to identify additional pertinent articles. The following keywords were used: stroke/hemiplegia/hemiparesis/cerebrovascular accident; electric/electrical; stimulation/nerve stimulation; afferent/sensory/somatosensory. The full text of articles identified by the title and/or abstract as possibly relevant were retrieved and final decision on inclusion was made by both researchers.

Inclusion Criteria

Study design

Studies included were randomized or quasi-randomized controlled trials (quasi-RCTs) in which patients were treated with sensory TENS to enhance motor recovery following a cerebral vascular accident. We included studies in which participants were assigned to 1 of 2 or more treatment groups involving a comparison between the effects of stimulation and control or placebo conditions. Studies in which none of the treatment groups consisted of sensory stimulation alone were excluded as such a design could not isolate the effect of sensory stimulation.

Study population

Studies were included if the study participants were diagnosed with either ischemic or hemorrhagic stroke, with no limitation as to the amount of time elapsed since the insult, its location, or its size.

Intervention

The intervention of interest was peripheral electrical stimulation applied to the skin via external electrodes at a sensory or subthreshold level but not at a level inducing muscle contraction. Although electrical stimulation via skin electrodes at a sensory level is usually termed TENS, previous reviews have revealed that authors use varying terminologies.¹⁹ For example, the term TENS is occasionally also used to describe electrical stimulation that produces a muscle contraction, whereas the generic term electrical stimulation may or may not be limited to sensory stimulation or to skin electrodes. We therefore did not limit the search to studies using the term TENS. On the other hand, studies using this term or the term sensory stimulation were excluded if it was noted that the stimulation was increased to a level that produced visible muscle contractions. Acupuncture treatments using sensory electrical stimulation were also identified by the search. Whereas the majority of these studies used needle electrodes and were thus excluded, studies using surface electrodes applied for sensory stimulation at acupuncture points were included.

Outcome measures

No limits were set as to outcome measures used to determine motor impairment and/or functional performance. However, we excluded studies that focused on the effect of sensory electrical stimulation on any of the following impairments without additional measures of motor recovery: dysphagia, neglect, pain, sensory perception, or spasticity.

Methodological Quality

The methodological quality of the included studies was graded independently by the 2 researchers using the PEDro Scale, which was developed by the Centre for Evidence Based Practice in Australia.²⁰ The scale was developed on the basis of expert consensus as to the determinants of the quality of RCT and has been shown to have good validity and reliability.^21,22 It consists of 10 items leading to a maximal score of 10. Points are allocated for randomization (random and concealed allocation), data reporting (baseline similarity, number of participants reported and assessed, between-group statistical comparison of at least 1 key outcome measure, and point and variability estimates), blinding (participants, therapists, and evaluators), and intention to treat. Although reporting of eligibility criteria is also noted, it is not included in the total PEDro score. Studies were rated between excellent and poor on the basis of the PEDro score, as follows: 9 to 10, excellent; 6 to 8, good; 4 to 5, fair; <4, poor. Discrepancies between the graders were resolved by mutual agreement.

In addition, all studies were graded according to the therapy/prevention arm of the Oxford Centre for Evidence-Based Medicine levels of Evidence.²³ Accordingly, levels of evidence were classified as follows: 1a, systematic review of RCT; 1b, RCTs with narrow confidence interval; 1c, all-or-none case series; 2a, systematic review cohort studies; 2b, cohort study/low quality RCT; 2c, outcomes research; 3a, systematic review of case-controlled studies; 3b, case-controlled study; 4, case series, poor cohort case controlled; expert opinion.

Data Extraction and Analysis

Data from the retrieved studies were extracted independently by both researchers on the following topics: patient age, time elapsed since stroke, research design, treatment characteristics, and treatment effects. The various outcome measures were classified in accordance with the health dimensions addressed by the International Classification of Functioning Disability and Health.²⁴ MetaAnalyst software was used to perform meta-analysis where appropriate, sufficiently homogeneous data concerning performance were available.²⁵ When sufficient data were not reported to enable calculation of the effect size, the relevant author was contacted, and the necessary data were requested. Effect size (Hedges G) was determined conservatively, based on comparisons of the final outcomes of treatment and control groups, using standardized scores and continuous random (DerSimonian-Laird) analysis while assuming unequal variances.

Results

Selection of the Literature

The preliminary search in PubMed, using the different combinations of keywords and limited to the English language, yielded 455 titles. Only 15 of these were identified as relevant to the present review. Excluded titles were related to functional electric stimulation, electrical stimulation that induces muscle contraction, outcome measures not in the inclusion criteria, acupuncture treatments, needle or implanted stimulation, single-subject design, and other nonrelated titles. No additional titles were retrieved from the remaining databases. Characteristics of the retrieved studies are summarized in Table 1 and Table 2 (online).

Table 1.

Participant Characteristics, Outcome Measures, and Treatment Effects

		Experimental Group (ExG)			Control Group (CG)
Study	Study Design	No. of Participants	Mean Age (SD), y	Stroke Duration	No. of Participants	Mean Age (SD), y	Stroke Duration	Test Time, Follow-up (FU)	Outcome Measures and ICF Level	Significant Effects
Levin and Hui-Chan³⁴	Two group; pre–post	11	58.5 (14.7)	26.4 (21.9) months	6	64.7 (10.6)	29.2 (17.2) months	Post 2 and 3 weeks; no FU	Body structure and function: clinical and EMG measure of spasticity; MVC dorsiflexion and plantar flexion	ExG, ↓ spasticity; ExG, ↑ dorsiflexion force
Tekeoglu et al⁴⁰	Two group; pre–post	30	55.9 (7.0)	40.8 (11.4) days	30	52.2 (5.4)	44.3 (13.1) days	Pre and post; no FU	Body structure and function: spasticity, Ashworth; Activity: Barthel Index	ExG, ↓ spasticity; ExG>CG, ↑ in total score
Conforto et al³¹	Crossover design	8	65.0 (range 38-81)	5.5 years (range 14 months to 7years)	Same as ExG crossover design			Pre and post each Rx session; no FU	Body structure and function: pinch strength	Active Rx, ↑ gain correlated with stimulation intensity
Peurala et al³⁹	Three group; pre–post test	32 UE; 19 LE	54.4 (10.0)	3.3 years (range 7 months to 14 years)	8 UE	Demographic data of ExG combined with CG		Pre and post; no FU	Body structure and function: skin sensation; SEPs Activity: MMAS; limb function; 10-m walk test	ExG, ↑ sensation ExG, ↑ SEPs ExG, ↑ MMAS ExG, ↑ function ExG, ↑ velocity
Chen et al²⁸	Two group; pre–post test	12	57 (Range 41-69)	Range 12-25 months	12	Computed with ExG	Computed with ExG	Pre and post; no FU	Body structure and function: Modified Ashworth 3 EMG measures of spasticity Activity: 10-m walk test	ExG, “trend” ↓ spasticity ExG, ↑ velocity
Wu et al³⁷	Crossover design	9	64.5 (4.4)	6.5 (1.0) years	Same as ExG; crossover design			Pre–post each Rx session; no FU	Activity: JTHFT	Active Rx, ↑ JTHFT; greater effect in more involved UE
Conforto et al²⁹	Crossover design	11	39.9 (4.2)	4.3 (0.7) years	Same as ExG; crossover design			Pre, post, and after JTHFT motor training in each Rx session; 30 day FU	Activity: JTHFT	ExG ↑ > CG ↑; greater gains maintained for 30 days when JTHFT motor training followed active Rx in second session
Yavuzer et al³⁸	Two group; pre–post test	15	61.9 (10.1)	3.5 (2.1) months	15	64.4 (9.8)	3.4 (2.3) months	Pre and post; no FU	Body structure and function: Brunnstrom stage; Activity: gait velocity, gait kinematics	ExG ↑ = CG ↑, in all measures
Ng and Hui-Chan³⁵	Four group; pre–post test	ExG1: 19 ExG2: 21	ExG1: 56.4 (9.1); ExG2: 58.4(7.1)	ExG1: 6.2 (4.1) years; ExG2: 5.0 (3.0) years	CG1: 20 CG2: 20	CG1: 57.1 (7.8) CG2: 57.3 (8.6)	CG1: 4.7 (4.1) years CG2: 5.2 (2.9) years	Pre, midperiod, post; 4-week FU	Body structure and function: spasticity (CSS); ankle peak torque Activity: gait velocity	ExG2 ↓ > CG1 ↓ ExG2 ↑ > ExG1 ↑ ExG2 ↑ > ExG1 ↑ ExG2 ↑ > CG1 ↑ ExG2 ↑ > CG2
Celnik et al²⁷	Crossover design	9	55.2 (14.3)	3.2 (1.6) years	Same as ExG crossover design			Pre and 1-hour following JTHFT training; 24-hour FU	Body structure and function: TMS, intracranial inhibition Activity: JTHFT	ExG1 ↓ ExG ↑ at post test and FU
Conforto et al³¹	Two group; pre–post test	11	59.3 (1.4)	53.1 (1.8) Days	11	64.2 (3.7)	53.5 (2.6) Days	Pre and post; 2- and 3-month FU	Body structure and function: Pinch- force; TMS Activity: FIM; JTHFT	No change No change No change ExG ↑= CG ↑ ExG ↑>CG ↑ Group difference decreased at FU
Klaiput and Kitisomprayoonkul³²	Two group; pre–post test	10	63.0 (11.1)	11.9 (10.6) days	10	64.5 (11.0)	38.9 (54.1) days	Pre and post	Body structure and function: lateral and tip pinch force Activity: ARAT	ExG ↑ > CG ↑ No change
Koesler et al³³	Crossover design	12	67.4 (6.4)	15.7 (4.2) months	Same as ExG crossover design			Two pre baseline tests and post	Activity: finger and hand tapping frequency; wrist and finger velocity	ExG ↑ ExG ↑
Yan and Hui-Chan²⁶	Three group; pre–post test and FU	19	68.4 (9.6)	9.2 (4.4) days	CG1: 19 CG2: 18	CG1: 72.8 (7.4) CG2: 70.4 (7.6)	CG1: 9.9 (2.6) days CG2: 8.7 (3.3) days	Pre, midperiod, post; 8-week FU	Body structure and function: spasticity (CSS); dorsiflexion, maximum torque; co-contraction ratio Activity: Timed Up and Go; days to independent gait	ExG ↑ > CG ExG ↑ > CG ExG1 ↓ > CG No group difference ExG tendency to walk earlier
Ng and Hui-Chan³⁶	Four group; pre–post test and FU	ExG1: 28 ExG2: 27	ExG1: 56.5 (8.2) ExG2: 57.8 (7.3)	ExG1: 4.9 (3.9) years ExG2: 4.7 (2.8) years	CG1: 25 CG2: 29	CG1: 56.9 (8.6) CG2: 55.5 (8.0)	CG1: 4.3 (3.8) years CG2: 5.0 (3.0) years	Prestimulation, mid and post Rx; 4-week FU	Activity: gait velocity; 6-minute walk; Timed Up and Go	ExG2↑ > all groups (by week 2 and at FU) ExG2↑ > CG1 and CG2 (at 2 weeks and FU); ExG1↑ > CG2 (at 4 weeks) ExG2↑ > all groups (by week 2, and at FU)

Abbreviations: ExG, experimental group; CG, control group; SD, standard deviation; FU, follow-up; ICF, International Classification of Functioning, Disability and Health; EMG, electromyography; MVC, maximum voluntary contraction; Rx, treatment; UE, upper extremity; SEPs, somatosensory evoked potentials; MMAS, Modified Motor Assessment Scale; JTHFT, Jebsen-Taylor Hand Function test; CSS, Composite Spasticity Scale; TMS, transcranial magnetic stimulation; FIM, Functional Independence Measure; ARAT, Action Reach Arm Test.

Methodological Quality

Quality rating scores based on the PEDro classification as well as evidence level of each study are presented in Table 3 (online). The mean (standard deviation) PEDro score was 6.9 (1.2). Whereas only 1 of the studies was graded as excellent (score of 9),²⁶ the majority of the studies were graded as good, with scores ranging between 6 and 8.^27-38 Only 2 studies were graded as fair (score of 5).^39,40 Two items were scored positively in only 1 or 2 studies (blind therapist²⁶ and concealed allocation, respectively),^32,36 whereas all the other items were scored positively in at least 10 studies. In terms of research design, 5 studies used a repeated-measures crossover design,^{27,29,31,33,37} 4 studies allocated the participants to more than 2 groups,^26,35,36,39 and 6 studies involved a 2-group comparison.^{28,30,32,34,38,40} With the exception of 1 study,³⁹ the number of participants per group was well balanced. Evidence level ranged between 1b and 3b, which is not surprising, because case studies were excluded a priori, and no expert opinion has been published on the topic. Evidence level of the majority of the studies was 2b or 3b, with only 4 articles involving rather large RCTs designated at evidence level 1b.^26,35,36,38 Upper-extremity (UE) rehabilitation, whether in the acute^30,32,40 or chronic^{27,29,31,33,37,39} stage was addressed by studies at evidence level 2b or 3b, with all studies indicating a positive effect on at least 1 outcome measure. Similarly, lower-extremity (LE) rehabilitation at the chronic stage was addressed by 2 studies at evidence level 1b^35,36 and 2 at level 2b,^28,34 indicating some positive outcomes. LE rehabilitation at the acute/subacute stage was addressed by only 2 studies at the 1b level^26,38 with only 1 of them demonstrating a positive effect.

Participants

The retrieved studies included a total of 446 patients, with 263 of them treated by sensory stimulation. (It should be noted that as the study reported by Ng and Hui-Chan in 2009³⁶ was an extension of their earlier study,³⁵ only the patients reported in 2009 were tallied. The effect on gait velocity, which was reported in both studies, was considered only in the later study.) The number of patients per study receiving active treatment ranged between 8 and 51, and the number receiving sham or control treatment ranged between 8 and 29. However, in the majority of studies (9/15), the number of participants receiving sensory stimulation was <15.

In 1 study, where TENS was applied to the LE, patients were in the acute phase of recovery,²⁶ and in 1 study, which involved the UE, patients were both in the acute and subacute stages of recovery.³² Three studies involving treatment of the UE and/or LE were conducted with patients in the subacute stage.^30,38,40 However, the majority of studies involved patients in the chronic stage of recovery, and 6 of these studies applied the TENS to the UE^{27,29,31,33,37,39} and 4 to the LE.^28,34-36

Intervention

No adverse effects were reported following any of the interventions. The method of stimulation varied to a great extent between studies in terms of location, pulse characteristics, intensity, and duration of the stimulation.

Location

In 1 study, TENS was applied to both the LE and the UE,⁴⁰ whereas in another study, it was applied to the UE in some of the patients and to the LE in others.³⁹ However, in 7 of the studies, the stimulation was applied solely to the UE^27,29-33,37and in 6 studies solely to the LE.^{26,28,34-36,38}

In 7 of the 9 studies involving the UE, the surface electrodes were positioned over the median nerve at the wrist.^27,29-33,37 In 2 of these studies, ulnar nerve stimulation was also induced,^27,32 and in another study, stimulation was applied to the median, ulnar, and radial nerves.³⁷ Only 1 UE study focused on stimulating the triceps brachii muscle, using electrodes to cover the muscle.⁴⁰ Unlike most studies that used relatively small electrodes, 1 study used a glove-like electrode to provide sensory stimulation to the entire hand and a sock-like electrode to likewise stimulate the entire foot.³⁹

As for the studies involving stimulation to the LE, placement of the electrodes was over the junction of the gastrocnemius muscle and Achilles tendon in 1 study,²⁸ over the common peroneal nerve in 3 studies,^34,38,40 and over 4 acupuncture points, related to LE function following traditional Chinese medicine, in 3 studies.^26,35,36

Pulse characteristics

Pulse shape characteristics were not reported in 8 of the studies^{26,27,29-33,37} and varied in the remaining studies. Pulse duration ranged from 0.125 ms to 1 ms, with 7 of the studies employing the 1-ms-long duration^26,29-33,37 and the other 8 studies using durations shorter than 0.240 ms.^{26,28,34-36,38-40} Pulse frequency ranged between 10 and 100 Hz. The most often used frequency was 10 Hz, delivered in 1-Hz pulse trains (5 pulses per train),^27,29-33,37 and the next most often used frequency was 100 Hz.^26,34-36 All studies used continuous stimulation, with the exception of the study by Yavuzer et al,³⁸ which used a 10-s on, 10-s off duty cycle.

Intensity of stimulation

Although current intensity (in mA) correlates with the level of sensation perceived by the patient, it cannot be used alone as an absolute determinant of perceived sensation because factors such as skin conductivity, location, and size of the electrode will also affect the level of sensation.¹⁶ Therefore, intensity was in most cases defined in terms of induced sensation, which varied between studies. In the studies by Peurala et al³⁹ and Conforto et al,³⁰ the current intensity was raised to a level just below sensory threshold. In 3 of the studies, the current intensity was double the level necessary to reach threshold perception.^34-36 Sensation induced in the remaining studies ranged from mild paresthesias (or tingling) to strong paresthesias, with all studies maintaining stimulation below the pain threshold and below visible motor contraction. In 5 of these studies, EMG (electromyography) was used to ensure that no muscle contractions were involved.^27,29-31,33

Duration of treatment

In 5 of the studies, all involving the UE, treatment was provided in a single 2-hour-long session.^29,31-33,37 In another similar study involving the UE, the stimulation was provided in two 2-hour sessions, whereby the ulnar and median nerves were stimulated simultaneously in 1 session and alternatively in the other.²⁷ All other studies used multiple treatment sessions, with the duration of treatments ranging between 20 and 120 minutes, the frequency of sessions per week ranging between 2 and 6, and the number of treatment weeks ranging between 3 and 8. Thus, the total number of treatment hours of studies using multiple treatments ranged from 8 hours²⁸ to 24 hours,²⁸ with a mean of 15.5 hours.

Control group treatment

In the majority of studies, the control groups were led to believe that they were receiving treatment, but the current intensity was actually maintained close to or at zero.^{26,27,29,32,34-36,38-40} However, in 4 studies, the control group received sensory stimulation at levels similar to those used in some of the studies as active treatment. Thus, stimulation of the control group ranged from the subsensory threshold level²⁹ to minimal perception,³² to the subparesthesia level,³¹ and to strong suprasensory stimulation.³⁰ Whereas most studies included only 1 control group receiving placebo treatment, in 1 study, the control group received no treatment.³³ In 1 study, control treatment was provided by stimulating the LE, whereas the intervention focus was actually on the UE function.³⁷ Additionally, 4 of the studies used 2 control groups, with one receiving placebo stimulation and the other no treatment.^26,35-37

Assessment

Whereas the participants in all studies were assessed both pretreatment and posttreatment, follow-up assessment was conducted in only 6 of the studies,^{26,27,29,30,35,36} with follow-up time ranging from 24 hours²⁷ to 3 months.³⁰ A wide variety of outcome measures was used to examine treatment effect. In reference to the model of the International Classification of Functioning, none of the studies examined the effect on aspects of the person’s participation, whereas measures of body structure/function and activity were used in similar frequency.

The body structure/function most frequently addressed was spasticity, with 2 of the studies using EMG^28,34 and 5 studies using a variety of clinical tools to assess it.²⁶ The next most frequently addressed body function was force, with 3 studies examining UE force^30-32 and 3 examining LE force.^34,35,39 The activity most often addressed was gait velocity.^{26,28,35,36,38,39} However, different studies measured velocity through a variety of activities, such as a 10-m walk, a 6-minute walk, or the Timed Up and Go test. The UE activity measure most commonly used was the Jebsen-Taylor Hand Function Test.^27,29,30,37

Treatment Effect

A summary of treatment effects reported in the various studies is presented in Table 1 (last column). Effect sizes and 95% confidence interval of the primary outcome measures, and the pooled effects computed when data were available for more than 1 study are presented in Table 4 (online). The P values reported in the original studies are included in this table whenever insufficient data were available to calculate the effect size.

Body structure and function domain

Only 1 study examined the effect of TENS on UE movement kinematics during reaching. Although the results showed a significant effect on wrist and finger velocity (P < .01), the study did not provide sufficient data to calculate effect size.³³ The single study examining the impact of TENS on LE movement kinematics reported no significant effect on spatial and temporal measures of gait or on LE range of motion during gait.³⁸

Pinch force was found to be favorably affected by TENS in 2^31,32 out of 3 studies.³⁰ However, the effect on pinch force could be pooled from only 2 of these studies,^30,32 indicating no significant effect of TENS on this measure. Although the effect of TENS on LE force production was measured for both dorsiflexion and plantar flexion, significant effects were reported only for dorsiflexion. Pooling the results of 3 studies, the meta-analysis indicates a significant favorable effect of TENS on the dorsiflexion force.^26,34,35 Finally, only 1 study used a global impairment scale (Brunnstrom Scale) to examine the effect of TENS on overall impairment level, indicating no significant effect.³⁸

Activity domain

The 10-m gait velocity test was the measure most frequently used to assess gait function.^28,36,38,39 Whereas 3 of these studies indicated a significant improvement in the experimental group treated with sensory TENS, the effect size analysis and meta-analysis of 3 of these studies indicate no significant effect on this measure.^28,36,38 Similar results were obtained regarding walking endurance, as measured by the 6-minute walk test³⁶ and regarding days to independent gait.²⁶ In contrast, the pooled effect on the Timed Up and Go test from 2 studies shows a significant result in favor of the experimental group.^26,36

The Jebsen-Taylor Hand Function Test (JTHFT) was the most frequently used measure to assess UE function, with 4 studies using this measure.^27,29,30,37 Whereas all studies reported a significant effect on the JTHFT, the data from 2 of these studies were not available to determine the effect size.^29,37 The pooled effect of the 2 remaining studies, though not significant, indicates a positive tendency.^27,30

The effect of TENS on finger and hand tapping frequency was evaluated in 1 study, with the results indicating a significant effect on finger tapping but no effect on hand tapping.³³ However, data were not available to determine the effect size. The Action Research Arm Test, which was used in 1 study to determine the effect on UE overall function, indicated no effect.³² Finally, the effect of TENS on the general activity level was assessed in 3 studies.^30,39,40 Different outcome measures were used in each study and thus could not be pooled. Although a significant treatment effect was reported for both the Barthel Index⁴⁰ and the Modified Motor Assessment Scale,³⁹ analysis indicates a significant effect size only for the Barthel Index.⁴⁰

Discussion

In all, 15 randomized or quasi-RCTs examining the effects of sensory TENS on motor recovery following a stroke were identified in the literature. All but 1 study,³⁸ which addressed LE function in the acute phase of rehabilitation reported statistically significant effects of sensory TENS on at least 1 aspect of motor performance (see Table 1). Yet because of the small number of participants per study and the large variability between them, the effect size analysis indicates a nonsignificant effect for most variables Moreover, the great variability between studies in terms of the outcome measures used as well as the insufficient data reported in some of the studies limited our ability to perform a meta-analysis. Thus, data for only 5 outcome measures could be pooled from 2 to 3 studies per outcome measure. The meta-analysis failed to show a favorable effect on gait velocity and pinch force. However, it indicates a significant effect of sensory stimulation to the LE on functional balance, as assessed by the Timed Up and Go test, and on force production of ankle dorsiflexion. Additionally, the pooling of data of only 2 of the 4 studies that demonstrated a significant effect on the JTHFT strongly suggests a positive impact of TENS on hand function as well.

The overall methodological quality of the retrieved studies, as evaluated using the PEDro classification, was good, with most items of the scale rated positively by the majority of the studies. However, some additional important features of the research methodology, which are not covered by the PEDro classification, also affect the ability to reach definitive conclusions regarding the effectiveness of sensory TENS. The 2 most important factors in this regard are the number of participants per study and the time span of the follow-up assessment. Whereas the number of participants per treatment group was between 8 and 51, the majority of studies, and in particular those with the more robust research methodology, involved a relatively small number of participants per treatment arm. Thus, the evidence level of most studies ranged between 2b and 3b. This resulted in insufficient power necessary to demonstrate effectiveness in at least some of the studies. Moreover, the small number of participants per study did not allow for their stratification by the severity of involvement or by lesion site—factors that have been shown to be significant determinants of the effectiveness of various treatments poststroke.^41,42

Only 6 studies included a follow-up assessment that ranged from 24 hours²⁷ to 3 months.^{26,29,30,35,36} Whereas 5 of them indicate that the various gains achieved by sensory TENS were maintained in the follow-up assessment, Conforto et al³⁰ reported that the significant improvement noted in hand function (JTHFT) after 4 weeks of sensory stimulation was not maintained after the cessation of treatment. It is not possible from the data reviewed here to determine the cause of these differences in results because of the varying stages of recovery between the sample populations as well as the different stimulation protocols used in the studies.

Nevertheless, it seems that the use of active practice in conjunction with sensory stimulation is an important determining feature. In 1 study with a positive long-term effect, which used a crossover design and involved only a single session of sensory TENS, gains in JTHFT were maintained for 30 days only when motor training was combined with active stimulation (and not placebo treatment) in the second of the 2 sessions.²⁹ In other studies, Ng and Hui-Chan^35,36 reported greater effects of sensory stimulation on gait velocity, the Timed Up and Go test, and ankle force production when active stimulation was combined with motor treatment as compared with using sensory TENS alone. However, given the small number of studies examining long-term effects and their contradictory results, further research is necessary to determine how best to facilitate the consolidation of the contribution of sensory stimulation to enduring cortical reorganization and to gains in motor performance.

Although all the reviewed studies used TENS to enhance peripheral sensory input, there was a high degree of variability between the studies in terms of the location of the electrodes, the duration of the treatments, and the stimulation characteristics. Thus, for example, whereas the majority of studies placed the electrodes over either specific muscles or nerves relevant to the impairment or activity assessed, others located them over acupuncture points.^26,35,36 Generally, the application of electrodes over the peripheral nerves will induce widespread sensation along the nerve’s distribution and corresponding cortical activation. Yet some of the studies that placed the electrodes over the muscle belly used large electrodes (eg, a glove) that covered the entire distribution of more than 1 peripheral nerve.³⁹ As stimulation directly over the peripheral nerve or over the muscle belly generates very similar sensations, which are mediated by peripheral sensory nerve endings, a similar physiological mechanism may be expected for both techniques. Furthermore, studies examining the effect of pain modulation via sensory TENS have shown similar effects when TENS application was over the painful area versus over acupuncture points along the same peripheral nerve⁴³ or even over extrasegmental points (ie, remote acupuncture points).⁴⁴ Nevertheless, future studies are necessary to determine whether the physiological mechanism determining the effectiveness of sensory TENS on motor recovery is dependent on electrode location and size.

Using transcranial magnetic stimulation, it was recently demonstrated in nonimpaired individuals that 3 weeks of daily sensory TENS to the abductor pollicis brevis resulted in a global widespread effect on the motor map representations of the hand and forearm muscles that extended beyond the stimulated median nerve distribution.¹¹ This finding indicates that the effect of stimulation may extend beyond the specific stimulated muscle. However, future research is necessary to determine the optimal site of stimulation, particularly as rehabilitation goals usually involve the acquisition of functional abilities that require the coordinated activation of multiple muscle groups.

The differences in the stimulation intensity used in different studies and their contradictory effects are particularly striking. In a recent study conducted by Conforto et al,³⁰ which included patients in the subacute stage following a stroke, it was demonstrated that repeated sessions of TENS delivered at a subthreshold intensity over a period of 1 month enhanced hand function (as measured by the JTHFT), whereas higher intensity (ie, suprasensory) TENS did not affect performance. These results are in contrast to previous single-session studies of patients in both the acute³² and chronic stages of recovery,^27,33,37 which used similar stimulation parameters in terms of site of application as well as pulse frequency and duration. Those studies demonstrated better hand function when TENS was delivered at a higher stimulation intensity rather than at a subthreshold level. In fact, some studies used a subthreshold intensity as their control treatment.³⁴ At this stage, it is impossible to determine the factors responsible for these contradictory results and what role current intensity plays. Indeed, it remains to be seen whether optimal current intensity is determined by the number of stimulation sessions (ie, single session vs multiple sessions), by the amount of time elapsed since the insult, or by other confounding factors influencing responsiveness to different intensities.

In a series of experiments with healthy participants, it was demonstrated that reorganization of the human motor cortex in response to sensory TENS is dependent, among other factors, on the frequency of stimulation. Stimulation at 1 to 5 Hz was shown to increase cortical excitation, whereas stimulation at 10 to 40 Hz was found to decrease it.⁴⁵ A study of healthy participants also demonstrated that the pattern of pulse frequency may play a role in spinally mediated plasticity. Comparing the effect on reciprocal inhibition, it was shown that 10 pulses at 100 Hz delivered intermittently every 1.5 s was more effective than continuous stimulation delivered at a high frequency (approximately 360 Hz).⁴⁶ This may suggest that stimulation is more beneficial if delivered at a physiological-like rate rather than continuously.

In the present review, both types of frequency delivery were used. The majority of studies of the UE used 5 pulse trains delivered once a second,^27,30-33,37 whereas the remaining studies used continuous stimulation delivered at frequencies ranging between 20 and 100 Hz. As most studies demonstrated some positive effects, it is impossible to draw any conclusions here about the relative contribution of stimulation frequency to enhanced motor recovery. Yet it is interesting to note that the only study that reported no advantage to sensory TENS used a completely different mode of stimulation delivery, with a continuous pulse frequency (at 35 Hz) that was delivered in a 10-s on, 10-s off duty cycle.³⁸ Whether this is a crucial factor determining the lack of observed effect in this study cannot be resolved on the basis of this review.

The present review indicates that sensory TENS may enhance motor recovery following a stroke, particularly when used in combination with active training. However, as the majority of the reviewed studies involved patients in the chronic stage of recovery, it has yet to be determined whether sensory TENS would be equally beneficial if used earlier during the rehabilitation process. It is also unclear as to what role location of the insult and severity of the deficits play in the responsiveness to sensory stimulation. Furthermore, given the great variability between studies in terms of stimulation parameters, further research is necessary to determine the effect of factors such as electrode location and stimulation parameters on long-term functional recovery of patients in both the acute and chronic stages of rehabilitation. Nevertheless, given the positive results reported by the majority of the reviewed studies, combined with the fact that TENS is relatively risk free and easy to implement, this modality when combined with active training seems to have potential as a noninvasive intervention that can enhance the benefits of customary rehabilitation treatments.

Footnotes

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

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

References

Asanuma

Pavlides

. Neurobiological basis of motor learning in mammals. Neuroreport. 1997;8:i-vi.

Pavlides

Miyashita

Asanuma

. Projection from the sensory to the motor cortex is important in learning motor skills in the monkey. J Neurophysiol. 1993;70:733-741.

Dobkin

. Do electrically stimulated sensory inputs and movements lead to long-term plasticity and rehabilitation gains? Curr Opin Neurol. 2003;16:685-691.

Han

Law-Gibson

Reding

. Key neurological impairments influence function-related group outcomes after stroke. Stroke. 2002;33:1920-1924.

Nudo

Friel

Delia

. Role of sensory deficits in motor impairments after injury to primary motor cortex. Neuropharmacology. 2000;39:733-742.

Hamdy

Rothwell

Aziz

Singh

Thompson

. Long-term reorganization of human motor cortex driven by short-term sensory stimulation. Nat Neurosci. 1998;1:64-68.

Floel

Hummel

Duque

Knecht

Cohen

. Influence of somatosensory input on interhemispheric interactions in patients with chronic stroke. Neurorehabil Neural Repair. 2008;22:477-485.

Cuypers

Levin

Thijs

Swinnen

Meesen

. Long-term TENS treatment improves tactile sensitivity in MS patients. Neurorehabil Neural Repair. 2010;24:420-427.

Ridding

Brouwer

Miles

Pitcher

Thompson

. Changes in muscle responses to stimulation of the motor cortex induced by peripheral nerve stimulation in human subjects. Exp Brain Res. 2000;131:135-143.

10.

Tinazzi

Zarattini

Valeriani

. Long-lasting modulation of human motor cortex following prolonged transcutaneous electrical nerve stimulation (TENS) of forearm muscles: evidence of reciprocal inhibition and facilitation. Exp Brain Res. 2005;161:457-464.

11.

Meesen

Cuypers

Rothwell

Swinnen

Levin

. The effect of long-term TENS on persistent neuroplastic changes in the human cerebral cortex [published online ahead of print June 9, 2010.]. Hum Brain Mapp. doi:10.1002/hbm.2107510.1002/hbm.21075.

12.

Castel-Lacanal

Marque

Tardy

. Induction of cortical plastic changes in wrist muscles by paired associative stimulation in the recovery phase of stroke patients. Neurorehabil Neural Repair. 2009;23:366-372.

13.

Johansson

Lindgren

Widner

Wiklund

Johansson

. Can sensory stimulation improve the functional outcome in stroke patients? Neurology. 1993;43:2189-2192.

14.

Lewis

Byblow

. The effects of repetitive proprioceptive stimulation on corticomotor representation in intact and hemiplegic individuals. Clin Neurophysiol. 2004;115: 765-773.

15.

Marconi

Filippi

Koch

. Long-term effects on cortical excitability and motor recovery induced by repeated muscle vibration in chronic stroke patients. Neurorehabil Neural Repair. 2011;25:48-60.

16.

Robertson

Ward

Low

Reed

. Electrotherapy Explained: Principles and Practice. Philadelphia, PA: Elsevier; 2004.

17.

DeSantana

Walsh

Vance

Rakel

Sluka

. Effectiveness of transcutaneous electrical nerve stimulation for treatment of hyperalgesia and pain. Curr Rheumatol Rep. 2008;10:492-499.

18.

Dubinsky

Miyasaki

. Assessment: efficacy of transcutaneous electric nerve stimulation in the treatment of pain in neurologic disorders (an evidence-based review): report of the Therapeutics and Technology Assessment Subcommittee of the American Academy of Neurology. Neurology. 2010;74: 173-176.

19.

Pomeroy

King

Pollock

Baily-Hallam

Langhorne

. Electrostimulation for promoting recovery of movement or functional ability after stroke. Cochrane Database Syst Rev. 2006;(2):CD003241.

20.

Sherrington

Herbert

Maher

Moseley

. PEDro: a database of randomized trials and systematic reviews in physiotherapy. Man Ther. 2000;5:223-226.

21.

Foley

Bhogal

Teasell

Bureau

Speechley

. Estimates of quality and reliability with the physiotherapy evidence-based database scale to assess the methodology of randomized controlled trials of pharmacological and nonpharmacological interventions. Phys Ther. 2006;86:817-824.

22.

Maher

Sherrington

Herbert

Moseley

Elkins

. Reliability of the PEDro scale for rating quality of randomized controlled trials. Phys Ther. 2003;83:713-721.

23.

Phillips

Ball

Sackett

. Levels of Evidence. Oxford, UK: Oxford Centre for Evidence-Based Medicine; 2009.

24.

World Health Organization (WHO). International Classification of Functioning, Disability and Health (ICF). Geneva, Switzerland: WHO; 2001.

25.

Wallace

Schmid

Lau

Trikalinos

. Meta-Analyst: software for meta-analysis of binary, continuous and diagnostic data. BMC Med Res Methodol. 2009;9:80.

26.

Yan

Hui-Chan

. Transcutaneous electrical stimulation on acupuncture points improves muscle function in subjects after acute stroke: a randomized controlled trial. J Rehabil Med. 2009;41:312-316.

27.

Celnik

Hummel

Harris-Love

Wolk

Cohen

. Somatosensory stimulation enhances the effects of training functional hand tasks in patients with chronic stroke. Arch Phys Med Rehabil. 2007;88:1369-1376.

28.

Chen

Lai

Chiang

Chen

. Effects of surface electrical stimulation on the muscle-tendon junction of spastic gastrocnemius in stroke patients. Disabil Rehabil. 2005;27:105-110.

29.

Conforto

Cohen

dos Santos

Scaff

Marie

. Effects of somatosensory stimulation on motor function in chronic cortico-subcortical strokes. J Neurol. 2007;254:333-339.

30.

Conforto

Ferreiro

Tomasi

. Effects of somatosensory stimulation on motor function after subacute stroke. Neurorehabil Neural Repair. 2010;24:263-272.

31.

Conforto

Kaelin-Lang

Cohen

. Increase in hand muscle strength of stroke patients after somatosensory stimulation. Ann Neurol. 2002;51:122-125.

32.

Klaiput

Kitisomprayoonkul

. Increased pinch strength in acute and subacute stroke patients after simultaneous median and ulnar sensory stimulation. Neurorehabil Neural Repair. 2009;23:351-356.

33.

Koesler

Dafotakis

Ameli

Fink

Nowak

. Electrical somatosensory stimulation improves movement kinematics of the affected hand following stroke. J Neurol Neurosurg Psychiatry. 2009;80:614-619.

34.

Levin

Hui-Chan

. Relief of hemiparetic spasticity by TENS is associated with improvement in reflex and voluntary motor functions. Electroencephalogr Clin Neurophysiol. 1992; 85:131-142.

35.

Hui-Chan

. Transcutaneous electrical nerve stimulation combined with task-related training improves lower limb functions in subjects with chronic stroke. Stroke. 2007;38: 2953-2959.

36.

Hui-Chan

. Does the use of TENS increase the effectiveness of exercise for improving walking after stroke? A randomized controlled clinical trial. Clin Rehabil. 2009;23: 1093-1103.

37.

Seo

Cohen

. Influence of electric somatosensory stimulation on paretic-hand function in chronic stroke. Arch Phys Med Rehabil. 2006;87:351-357.

38.

Yavuzer

Oken

Atay

Stam

. Effect of sensory-amplitude electric stimulation on motor recovery and gait kinematics after stroke: a randomized controlled study. Arch Phys Med Rehabil. 2007;88:710-714.

39.

Peurala

Pitkanen

Sivenius

Tarkka

. Cutaneous electrical stimulation may enhance sensorimotor recovery in chronic stroke. Clin Rehabil. 2002;16:709-716.

40.

Tekeoglu

Adak

Goksoy

. Effect of transcutaneous electrical nerve stimulation (TENS) on Barthel Activities of Daily Living (ADL) index score following stroke. Clin Rehabil. 1998;12:277-280.

41.

Hendricks

van Limbeek

Geurts

Zwarts

. Motor recovery after stroke: a systematic review of the literature. Arch Phys Med Rehabil. 2002;83:1629-1637.

42.

Kwakkel

Kollen

van der Grond

Prevo

. Probability of regaining dexterity in the flaccid upper limb: impact of severity of paresis and time since onset in acute stroke. Stroke. 2003;34:2181-2186.

43.

Cheing

Chan

. Influence of choice of electrical stimulation site on peripheral neurophysiological and hypoalgesic effects. J Rehabil Med. 2009;41:412-417.

44.

Chesterton

Barlas

Foster

Lundeberg

Wright

Baxter

. Sensory stimulation (TENS): effects of parameter manipulation on mechanical pain thresholds in healthy human subjects. Pain. 2002;99:253-262.

45.

Fraser

Power

Hamdy

. Driving plasticity in human adult motor cortex is associated with improved motor function after brain injury. Neuron. 2002;34:831-840.

46.

Perez

Field-Fote

Floeter

. Patterned sensory stimulation induces plasticity in reciprocal ia inhibition in humans. J Neurosci. 2003;23:2014-2018.

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

0.03 MB

0.04 MB