Clinical Rehabilitation 2009; 23: 2739

Evidence for the retraining of sensation after stroke: a systematic review

SM Schabrun Research Centre for Human Movement Control, Discipline of Physiology, School of Molecular and Biomedical Science, The University of Adelaide and S Hillier Centre for Allied Health Evidence, School of Health Sciences, The University of South Australia, Adelaide, Australia Received 5th July 2009; returned for revisions 19th August 2008; revised manuscript accepted 27th August 2008.

Objective: Retraining of sensory function following stroke is frequently overlooked in rehabilitation protocols despite more than 60% of patients presenting with sensory deficits. Methods to train sensory function include both passive and active training protocols. Here we examined the volume and quality of the evidence available for both passive and active sensory training following stroke. In addition, we aimed to quantify the effect of sensory training on impairment and function. Data sources: Databases searched included MEDLINE, AMED, CINAHL, Academic search elite, Scopus and the Cochrane library. Unpublished articles were identified using a search engine. Review methods: Studies utilizing passive or active sensory training paradigms post stroke were identified. Methodological quality was examined using the National Health and Medical Research Council hierarchy of evidence and the McMaster University critical appraisal tool. Results: Fourteen studies met the inclusion criteria; 8 examined passive and 6 active sensory training. Methodological quality scores ranged from 11 to 18.5 (maximum 20). Meta-analysis was performed using three studies examining hand function, demonstrating a moderate effect in favour of passive sensory training. Other studies were unable to be pooled due to heterogeneity of measures or insufficient data. Conclusion: Meta-analyses and single studies offer some support for the effectiveness of passive sensory training in relation to sensory impairment and motor function. However, empirical evidence for active sensory training is limited. Further high-quality studies with greater statistical power and meaningful clinical measures are required in order to accurately determine the effectiveness of sensory retraining following stroke.

Introduction
Address for correspondence: Siobhan Schabrun, Research Centre for Human Movement Control, Discipline of Physiology, School of Molecular and Biomedical Science, The University of Adelaide, Adelaide, SA 5005, Australia. e-mail: siobhan.schabrun@adelaide.edu.au SAGE Publications 2009 Los Angeles, London, New Delhi and Singapore

Stroke is a significant cause of disability, reduced independence and decreased quality of life worldwide. In fact less than half of patients regain functional use of the stroke affected upper limb despite ongoing rehabilitation.1 The ability to
10.1177/0269215508098897

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SM Schabrun and S Hillier Sensory training following stroke can occur using one of two methods. Passive sensory training involves the application of electrical stimulation to produce activation of cutaneous nerves in the absence of muscle contraction (e.g. Yavuzer and colleagues9). Conversely, active sensory training involves a series of exercises designed specifically to train sensory function, for example, practise localizing and detecting the position of body parts in space (e.g. Carey and collegues4). While it is thought that sensory training may improve not only sensory deficits but also motor impairment and function in those with stroke, the available literature on this topic has yet to be systematically evaluated. Thus the aims of the current review were first to evaluate the methodological quality of the available evidence for passive and active sensory training following stroke and second, to examine the effect of passive and active sensory training on impairment-specific and functional outcomes following stroke.

perform skilled motor movements and therefore function independently is closely correlated with the ability to accurately perceive and discriminate sensations of pain, temperature, pressure and vibration, as well as the ability to accurately locate body parts in space (proprioception).2 Yet sensation remains a poorly treated presentation in the clinical setting despite over 60% of stroke patients presenting with some form of sensory deficit.3 Sensory deficits following hemispheric stroke can result from damage to a number of cortical and subcortical structures, most notably to the primary somatosensory area situated in the postcentral gyrus.2 Damage resulting in decreased sensory awareness has a number of functional implications which can reduce an individuals ability to function independently and impact upon their quality of life. These include safety concerns, particularly around the detection of thermal sensations, impaired spontaneous use of the affected hand, an inability to sustain grasp and effectively manipulate objects and an impaired ability to reacquire skilled movements essential to accomplish activities of daily living.4,5 In addition, those with stroke frequently develop a learned non-use of their affected limb.4 Sensory deficits in stroke patients are of particular concern in light of recent neurophysiological research which demonstrates the importance of sensory input in maintaining normal cortical representations in both the sensory and motor cortices. For example, following the elimination of sensory input through amputation or nerve block, cortical regions adjacent to the deafferented region rapidly expand into the unused cortical territory.6 Several studies have demonstrated that tactile stimulation of the lip in subjects with deafferentation of the hand evokes cortical responses not only in the area of the face but also in the cortical region normally corresponding to the deafferented hand.6,7 These findings suggest that sensory input is likely to be integral to the preservation of cortical representations and therefore function in the upper limb following stroke. Indeed, it has been shown that changes in cortical representations accompany the functional gains seen in stroke patients following rehabilitation (see Richards and colleagues8 for review). Yet, despite these findings, sensory retraining following stroke is frequently overlooked in current rehabilitation protocols.

Methods
Literature review Published studies were identified using key search terms describing the target patient population (stroke) and the intervention (sensory training). The search strategy was run for all major databases including MEDLINE, AMED, CINAHL, Academic search elite, Scopus and the Cochrane library. Unpublished articles were identified using the search engine GOOGLE. In a final step, the reference lists and bibliographies of all relevant literature were hand searched. An example of the search strategy used in the MEDLINE database is shown in Appendix 1.

Included literature All literature were restricted to full-text publication in English, utilized an experimental design and reported original, primary data. No publication date limits were set. Unsuitable literature was excluded using titles, abstracts and where necessary full text.

Retraining of sensation after stroke

Table 1 Designation of National Health and Medical Research Council levels of evidence Study design

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Level of evidence I II III-1 III-2 III-3 IV

Evidence obtained from a systematic review of all relevant randomized controlled trials Evidence obtained from at least one properly designed randomized controlled trial Evidence obtained from well designed pseudo randomized controlled trials (alternate allocation or some other method) Evidence obtained from comparative studies (including systematic reviews of such studies) with concurrent controls and allocation not randomized, cohort studies, casecontrol studies or interrupted time series with a control group Evidence obtained from comparative studies with historical control, two or more single arm studies or interrupted time series without a parallel control group Evidence obtained from case series, either post-test or pre-test/post-test

 Patient population: Studies were included if the target population had suffered a stroke. No limits were applied to the type (infarct/ haemorrhage), anatomical location or stage (acute, semi-acute or chronic) of stroke evaluated. Literature involving animals or animal models was excluded.  Intervention: Sensory training (passive or active) applied to the upper or lower limb was required to be the sole experimental intervention. Studies which combined sensory training with other forms of therapy, or where sensory training was embedded within broader rehabilitation protocols, were excluded.  Passive sensory training: Articles were required to employ afferent stimulation protocols which did not produce muscle contraction (e.g. functional electrical stimulation), were not paired with other forms of electrical stimulation (e.g. paired associative stimulation) and were applied via surface electrodes with a clear intent to stimulate only somatosensory regions.  Active sensory training: Active sensory training was restricted to interventions with a clear intent to retrain only sensory function. Such interventions included exercises to specifically target sensory function, such as practise discriminating and localizing sensations, stereognosis and proprioception.  Outcomes: Studies were included if they measured outcomes relating to local sensory or motor impairments (e.g. sensory discrimination, range of motion, postural sway) or function (e.g. task-specific activities, ambulation) in the upper or lower limb.

Assessment of methodological quality Included studies were ranked according to the National Health and Medical Research Council (NHMRC) hierarchy of evidence (Table 1).10 Methodological quality was then assessed using a modified version of the quantitative critical appraisal tool developed by Law et al.11 To ensure rigorous examination of methodological quality the criterion concerning sample size was expanded to include the random selection of subjects, use of a control group, allocation concealment, relevant inclusion/exclusion criteria, adequate explanation of baseline characteristics and suitable blinding of subjects and therapists involved in treatment delivery and assessment of outcomes. This tool has been widely used in the systematic review process1214 and demonstrates good inter-rater reliability.11 The critical appraisal tool assessed six domains including study justification and design, sampling, outcome measures, methods, analysis methods and conclusions. Criteria which were adequately addressed scored the full number of points (1 or 0.5 depending on the criterion being evaluated), while criteria that were insufficiently reported or not stated received zero. Using this method the maximum score possible was 20. To ensure consistency, allocation to the NHMRC hierarchy and critical appraisal of all articles was performed by two independent assessors. Discrepancies were resolved by a third independent reviewer.

Data extraction and analysis Details from each study regarding the method (design, participants, intervention and outcome

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SM Schabrun and S Hillier contraction (N 11). The complete table of excluded studies is available from the authors.

measures) and the results (sample size, means and standard deviations) were extracted using a standardized form. Data from primary outcome measures relating to sensation, proprioception, strength, spasticity and function were extracted from each study. Review Manager software (RevMan5) was used to perform a meta-analysis where appropriate, sufficiently homogeneous data were available and to calculate effect sizes for single studies. Data were extracted and analysed to calculate relative risk, 95% confidence intervals (CI) and individual and group effect sizes. For evaluation of all dichotomous data, the number of participants in both the experimental and control group and the total sample size were identified. Continuous data were evaluated using the number of participants in each group plus the mean and standard deviation of the change score (post interventionpre intervention value) for each group. As the heterogeneity among studies was expected to be relatively high, all meta-analyses were calculated using random effects. Where data were not available or of unacceptable heterogeneity, a narrative summary of study results was produced using reported P-values. Where necessary, authors were requested to provide missing data.

Description of studies Level of evidence An absence of level I evidence was identified in both the passive and active sensory training literature. Among the eight passive training studies selected for review, three were classified as level II evidence,9,15,16 four as level III evidence1720 and one as level IV evidence.21 A similar distribution of evidence was present within the active sensory training literature. Two studies were verified as level II evidence,22,23, one as level III-2 evidence5 and three studies were classified as NHMRC level IV.4,24,25

Results
Identification and selection of studies The literature search resulted in the identification of 118 studies of which 14 were retained for inclusion in this review. Eight studies utilized a passive sensory training intervention and six an active sensory training intervention. Studies were excluded for the following reasons: descriptive papers (N 16); narrative review articles (N 20); studies evaluating outcome measurement tools, prognostic indicators or clinical models (N 18); studies evaluating interventions not related to passive or active sensory training (e.g. drug therapy, motor retraining, pneumatic compression, vibration training, thermal stimulation, ice immersion; N 25); studies examining interventions not confined to the upper or lower limb (e.g. cognition, speech, vision, sexual function, incontinence; N 14); and passive sensory training interventions which produced a muscle

Methodological quality Methodological quality was similar for both the passive and active sensory training literature. Studies examining passive sensory training interventions returned a mean standard deviation (SD) quality score of 13.7 1.6, while studies utilizing active sensory training paradigms returned a score of 13.7 2.8. Quality scores ranged from 114,21 to 18.5.22 The most common methodological inadequacies were failure to justify sample size (13), failure to conceal random allocation (13), absence of therapist blinding (12) and the use of outcome measures with undemonstrated reliability (8) and validity (10).

Participants A total of 199 stroke survivors received passive or active sensory training interventions across the 14 studies. A further 97 subjects acted as controls. Stroke duration ranged from 19 days to 16 years. Details of stroke type were absent for 168 subjects. However, where reporting did occur the majority of included subjects had suffered an ischaemic stroke (N 82). Lesion location was divided between the left hemisphere (N 145), right hemisphere (N 151) and subcortical structures (N 1). Nine studies examined the effect of sensory training in the upper limb, four in the lower limb and one study examined sensory training

Retraining of sensation after stroke applied to both the upper and lower limb. No adverse effects were reported from following any of the sensory training interventions. Further characteristics of included studies are detailed in Tables 2 and 3.

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Passive sensory training Interventions Cutaneous electrical stimulation was applied using a variety of frequency and intensity settings. Four studies used a 1 Hz train of five single pulses delivered at 10 Hz,15,17,20,21 two used a 35 Hz biphasic current,9,19 one a monophasic current delivered at 50 Hz,18 and one a square-shaped pulse delivered at 100 Hz.16 Intensities ranged from just below perceptual threshold to bearable pain. Control interventions consisted of cutaneous stimulation applied below perceptual threshold, and application of the cutaneous stimulation device with the machine turned on, but without current delivery. Training durations ranged from one 2-hour session15,17 to 30 minutes applied each day, five days a week, for eight weeks.16

experimental group (Table 4). Heterogeneity was acceptable. The single study by Yavuzer et al.9 also gave a significant result in favour of the experimental group for the Brunnstrom stages measure (SMD, fixed effects 0.67; 95% CI 0.25 to 1.09; P 0.002). The only other study21 with appropriate data failed to demonstrate any significant effects using hand dynamometry (SMD, fixed effects 3.5; 95% CI 8.13 to 1.13; P 0.14). The three studies that contained insufficient data to be included in the meta-analysis demonstrated mixed results. Tekeog lu and colleagues16 reported positive findings for the treatment of spasticity using the modified Ashworth Assessment of Spasticity Scale, but Sullivan and Hedman19 were equivocal on this measure. Functional improvements were reported using the Action Research Arm Test19 but not with the modified Motor Assessment Scale.18

Outcome measures Spasticity, motor function and gait were the most common outcomes assessed following passive sensory training. Spasticity was measured using the modified Ashworth Assessment of Spasticity Scale in two studies.16,19 Motor function was assessed using a range of scales including the Jebson-Taylor Hand Function Test,15,17,20 modified Motor Assessment Scale,18 Action Research Arm Test,19 Brunnstrom Stages9 and the Barthel Index.16 One study used an analysis of gait kinematics9 and another the 10-metre walk test to evaluate gait.18 One study evaluated strength using a dynamometer.21

Active sensory training Interventions Three studies used the active sensory training programme outlined in Yekutiel and Guttman.5 This protocol consisted of education, practice detecting, localizing and discriminating sensations and proprioceptive training.5,22,24 Two further studies used similar training protocols focusing on localization, sensory recognition and proprioception.4,25 The final study employed perceptual learning exercises consisting of a rubber hardness discrimination task.23 Control interventions included relaxation exercises. In addition to active sensory training, participants in three studies continued to receive standard care.4,22,23 Training duration varied from 30 to 50 minutes22,25 for each session and the number of sessions ranged from 6 to 30.24,25

Effect of passive sensory training Data for the Jebsen-Taylor Hand Function Test (JTHFT) were able to be pooled from the studies by Celnik et al.,15 Conforto et al.17 and Wu et al.20 The test for overall effect was 1.08 (standard mean difference (SMD), random effects) with 95% CI 0.52 to 1.64 (z 3.78, P 0.002) in favour of the

Outcome measures The key outcomes addressed were light touch, proprioception, function and postural sway. Four studies used Semmes-Weinstein monofilaments to assess light touch,4,22,24,25 while one study used a blunt pencil and asked subjects to identify the region of touch.5 Five of the six studies

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Table 2 Conforto et al. 200221 9E 64.5 (4.4) 5:4 6.5 (1) years FM 93 (1) 3.2 (1.6) years 4.3 (0.7) years 3:6 4:7 n/a 5 (4.1) years ARAT 20.2 (12.5) 51 E/8 C 54.4 (10) E n/a C 42:18 E n/a C 3.3 (n/a) years E n/a C 9E 55.2 (14.3) 11 E 39.9 (4.2) 9E 51.8 (10.2) Peurala et al. 200218 Wu et al. 200620 Celnik et al. 200715 Conforto Sullivan and et al. 200717 Hedman 200719

Passive sensory retraining: characteristics of included studies Yavuzer et al. 20079 15 E/15 C 61.9 (10) E 64.6 (9.8) C 7:8 E 9:6 C 3.5 (2.1) months E 3.4 (2.3) C FIM 72.3 (18.3) E 73.4 (16.6) C 35 Hz, 0.024 ms, sensory threshold 35 Hz, 0.025 ms, sensory threshold Median nerve Hand 12h 2 15 min/day session n/a n/a JTHFT 15.5 JTHFT 15 ARAT MAAS 12.5 CPN 1 30 min/day 5 days/4 weeks Sham stimulation

SM Schabrun and S Hillier

lu Tekeog et al. 199816

Sample size Age in years mean (SD) Gender M:F

30 E/30 C 8E 55.9 (7) E 65 (n/a) 52.2 (5.4) C 17:13 E 7:1 14:16 C 5.5 (n/a) Stroke duration 40.8 (11.4) years mean (SD) days E 44.3 (13.1) C Severity BI 30.4 (22.1) E Dynamometer mean (SD) 44.7 (17) C 49.7 (8.1) E 54.4 (10.6) C 100 Hz, 0.2 ms, 10 Hz, 1 ms, Frequency, bearable pain strong pulse length, paraesthesias intensity MMAS 33.7 (10) E FM 87.6 (2.2) Hand 26.6 (12) E Foot 31.7 (13) C 50 Hz, n/a, 10 Hz, 1 ms, subsensory mild paraesthesias Median nerve Hand 3 2 h sessions 1 2 h session n/a n/a JTHFT 13.5 FM median 65 (range 5666) 10 Hz, 1 ms, 10 Hz, 1 ms, strong mild paraesthesias paraesthesias

Target Duration

Control condition Outcome measures

CPN 1 30 min/day 5 days/8 weeks Sham stimulation BI, MAAS

Quality score

14

Median nerve Hand/foot 2 2 h sessions 2 20 min/day 3 weeks n/a Sham stimulation MMAS Muscle 10 m walk strength (dynamometer) 11 13

Brunnstrom stages, gait kinematics 15.5

E, experimental group; C, control group. n/a, data not available; MMAS, modified Motor Assessment Scale; ARAT, Action Research Arm Test; FM, Fugl-Myer Motor Assessment; FIM, Functional Independence Measure; BI, Barthel Index; CPN, common peroneal nerve; MAAS, modified Ashworth Assessment of Spasticity; JTHFT, Jebson-Taylor Hand Function Test.

Table 3 Yekutiel and Guttman 19935 4E 51.7 (13.4) 2:2 10 (6.9) months n/a Sensory practice, recognition ADLs n/a 3:0 42 years 3E 6373 range Morioka and Yagi 200323 Smania et al. 200325 Hillier and Dunsford 200624

Active sensory retraining: characteristics of included studies Lynch et al. 200722

Carey et al. 19934

Sample size Age in years mean (SD) Gender M:F Stroke duration mean (SD) Severity mean (SD)

8E 49.8 (15.8)

7:1 12.8 (7.1) weeks n/a

20 E/19 C 64 (n/a) E 67 (n/a) C 13:7 E 8:11 C 6.2 (n/a) years E 6.2 (n/a) C n/a

10 E/11 C 61 (15.8) E 62 (12.3) C 7:3 E 9:2 C 48.7 (31.1) days E 47.8 (27.7) C n/a

Intervention LL 10 days 2 weeks

Localization, proprioception

12 E/14 C 62.6 (13.3) E 61.3 (11) C 9:3 E 8:6 C 65.4 (18.6) days E 61.9 (20.8) C 2 point discrimination 6.6(4.6) E 7.2 (3.6) C Perceptual learning exercises Education, sensory practice, proprioception LL 45 min/session 3 sessions/week 2 weeks n/a SWM, PDT, ADLs 13 SWM, DPT 11.5

Target Duration

UL 10 sessions

Education, sensory practice, proprioception UL 45 min/session 3 /week 6 weeks n/a UL 50 min/session 30 sessions 1 hour home exercise n/a

Education, sensory practice, proprioception LL 30 min/session 10 sessions 2 weeks

Control condition

n/a

Outcome measures 15.5

SWM, PDT

Standard physiotherapy Stabilometer

Relaxation exercises SWM, DPT, BBS 18.5

Quality score

11

Touch localization, elbow position 13

Retraining of sensation after stroke 33

E, experimental group; C, control group; n/a, data not available; UL, upper limb; LL, lower limb; ADLs, activities of daily living; PDT, Proprioceptive Discrimination Test; DPT, Distal Proprioception Test; BBS, Berg Balance Scale; SWM, Semmes-Weinstein Monofilaments.

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SM Schabrun and S Hillier

Effects of passive sensory retraining on hand function, strength and spasticity Primary outcome measure Experimental gain n/a n/a 12.7 (19.8) Hand 5.03 (5.2) 14.2 (10.1) 4.1 (4.9) 0.93 (0.7) 1.1 (6.4) n/a 1.7 (9.4) Control gain n/a n/a 2.0 (6.6) 0.11 (2.9) 1.9 (10.1) n/a 0.26 (0.45) 2.4 (1.9) n/a n/a Reported effect 0 0 Mean difference (95% CI)

Table 4

Function Tekeog lu et al. 199816 Peurala et al. 200218 Wu et al. 200620 Celnik et al. 200715 Conforto et al. 200717 Sullivan and Hedman 200719 Yavuzer et al. 20079 Muscle strength Conforto et al. 200221 Spasticity Tekeog lu et al. 199816 Sullivan and Hedman 200719

BI MMAS JTHFT JTHFT JTHFT ARAT Brunnstrom stages Dynamometer MAAS MAAS

0.95 (0.04, 1.94)*# 1.11 (0.10, 2.12)*# 1.17 (0.25, 2.09)*# 0.67 (0.25,1.09)* 3.50 (8.13, 1.13)

n/a, data not available. *P50.05. # Combined in meta-analysis: total effect (95% CI) 8.72 (2.48, 14.95). Significant effects reported by individual studies (P50.05); 0, absence of significant effects reported by individual studies. MMAS, modified Motor Assessment Scale; ARAT, Action Research Arm Test; BI, Barthel Index; MAAS, modified Ashworth Assessment of Spasticity; JTHFT, Jebson-Taylor Hand Function Test.

examined proprioception. Both studies performed in the lower limb used the distal proprioception test.22,24 In the upper limb, two studies used the proprioceptive discrimination test designed by Carey and collegues4,25 and one study examined elbow position sense by blindfolding the patient, moving the plegic arm through a series of 10 angles and asking the subject to match each position with his other arm.5 Two studies examined the effect of active sensory retraining on function: the first using a series of activities of daily living25 and the second using the Berg Balance Scale.22 One study used a stabilometer to examine postural sway.23

Data from Morioka and Yagi23 also failed to demonstrate significant effect sizes for the stabilometer measure of postural control (P 0.30). Of the studies not included in the meta-analyses above, positive findings were reported for activities of daily living24 and tests of sensation,4,5,24,25 while equivocal results were reported for proprioception.4,24

Discussion
A small number of studies exist examining the effects of active and passive sensory training protocols on impairment and function post stroke. Passive sensory training was shown to have a significant beneficial effect on hand function including grip strength and hand dexterity as measured using the Jebsen-Taylor Hand Function Test. Further beneficial effects of passive sensory training on function were demonstrated by a significant effect size for an improvement in Brunnstrom stages and by the reported results of a single study demonstrating an improvement in Action Research Arm Test scores. There was no

Effect of active sensory training There were insufficient studies with appropriate data to allow pooling across studies (Table 5). Data from Lynch et al.22 were analysed for effect sizes. However, pooling of all cutaneous testing scores failed to reveal a significant overall effect (P 0.6). In addition, significant effects were not present for the Berg Balance Scale (P 0.57) or the distal proprioception test (P 0.92).

Retraining of sensation after stroke

Table 5 Effects of active sensory retraining on hand function, sensation and proprioception Primary outcome measure Function Smania et al. 200325 Morioka and Yagi 200323 Lynch et al. 200722 Sensation Yekutiel and Guttman 19935 Carey et al. 19934 Smania et al. 200325 Hillier and Dunsford 200624 Lynch et al. 200722 Proprioception Yekutiel and Guttman 19935 Carey et al. 19934 Smania et al. 200325 Hillier and Dunsford 200624 Lynch et al. 200722 ADLs Stabilometer (ENV) BBS Localisation SWM SWM SWM SWM lateral Medial Heel Elbow position PDT JPS DPT DPT Experimental gain n/a 2.3 (5.1) 5.1 (4.38) n/a n/a n/a n/a 1.09 (1.4) 0.21 (0.90) 0.52 (1.03) n/a n/a n/a n/a 0.5 (4.00) Control gain n/a 0.3 (4.6) 3.81 (5.96) n/a n/a n/a n/a 1.1 (1.28) 0.48 (1.28) 0.70 (1.07) n/a n/a n/a n/a 0.36 (2.57) Reported effect 0 0 0 0 0 0 0 0

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Mean difference (95% CI)

2.00 (1.76, 5.67) 1.29 (3.16, 5.74)

0.01 (0.85, 0.86) 0.23 (0.63, 1.09) 0.16 (0.69, 1.02)

0.14 (2.77, 3.05)

n/a, data unavailable. , significant effects reported by individual studies (P50.05); 0, absence of significant effects reported by individual studies. ADLs, activities of daily living; PDT, Proprioceptive Discrimination Test; DPT, Distal Proprioception Test; BBS, Berg Balance Scale; SWM, Semmes-Weinstein Monofilaments; ENV, enveloped area; JPS, joint position sense.

clear evidence for an effect of active sensory training on function, postural sway, cutaneous sensation or proprioception using a meta-analysis approach. Studies included in the current review were of varying design and methodological quality, making the drawing of sound conclusions regarding treatment efficacy difficult. Randomized controlled trials are considered the gold standard when determining treatment effectivness due to a robust methodological design, which minimizes the effects of bias.26 However, only 5 of the 14 studies met the criteria for high-level randomized controlled trials. The remaining 9 studies consisted of lower level pseudo randomized trials, comparative studies or case series designs. The diversity of designs is one factor likely to contribute to the observed inconsistencies in outcomes across studies. Methodological quality was reasonable across all studies. However, there were several areas where methodological rigor was notably lacking, introducing the potential for bias and reducing confidence in reported results. Of the 14 studies

included in this review only one provided justification for the chosen sample size.22 Failure to calculate and obtain an appropriate sample size increases the probability of returning a non-significant finding, even if a significant difference exists among the wider population.13 Thus, it is possible that the insufficient evidence found for sensory training after stroke is due to poor statistical power rather than an ineffective intervention. In addition, only a small number of studies included a specific control condition. Controlled trials are often limited by ethical issues surrounding the withdrawal or absence of standard treatment. However, it is possible for the intervention (e.g. electrical stimulation or sensory practice) and a control condition (e.g. sham stimulation or relaxation exercises) to be given in conjunction with standard care. This approach allows for the effects of the intervention to be clearly delineated from those relating to standard care. Research findings were also limited by the failure of 12 studies to blind the therapist, providing the treatment to group allocation. While therapist blinding is not without its complexities in clinical

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SM Schabrun and S Hillier improve hand function and dexterity in those with stroke. The use of passive sensory training to improve spasticity and muscle strength post stroke is less convincing. A number of single studies report positive effects on function, sensation and proprioception following active sensory training. However, the lack of sufficient data to perform meta-analysis and insignificant effect sizes mean it is not yet possible to determine the effectiveness of active sensory training in stroke rehabilitation. While the findings of this review suggest that passive sensory training is likely to be more beneficial than active training in producing functional gains post stroke, this discrepancy is likely to be the result of the lower level of evidence and use of inconsistent outcome measures present within the active sensory training literature. While 7 of 8 passive sensory training studies were classified as randomized or pseudo randomized controlled trials only 2 of 6 active sensory training studies met the same criteria. The presence of lower level designs, and the subsequent lack of control groups, prevented both meta-analysis and calculation of meaningful effect sizes for a number of studies. Further high-quality research is needed before any distinction can be made between the effects of passive and active sensory training and the mechanisms behind any such difference elucidated. It is noteworthy that the types of outcome measures used to assess improvements following passive and active sensory training interventions differed. Studies evaluating passive training predominantly used outcome measures relating to function, while those using active training focused on outcome measures at the impairment level such as touch localization and proprioception. It is possible that changes occurring at the impairment level are more difficult to detect. Changes in touch localization or proprioception are also more likely to be of a smaller magnitude and these values may not easily reach statistical significance. In contrast, improvements in function tend to be larger and may be the result of net improvements in sensation, proprioception and motor function rather than the result of improvements in one component. The choice of outcome measures may therefore have contributed to the results of this review.

research, failure to control for this form of bias may result in more intensive treatment being inadvertently received by the treatment group. While this effect can be controlled in those studies using passive sensory training interventions, where the duration and intensity of electrical stimulation is set in advance, this level of control is more difficult to achieve using active, and therefore therapist driven, sensory training. Confidence in reported results is further compounded by the inadequate, or unstated, reliability and validity of reported outcome measures. A large number of studies used outcome measures for which reliability and validity procedures have not been established. Furthermore, gross measures of functional change are unlikely to contain sufficient sensitivity to detect the localized changes resulting from sensory training. For example, the modified Motor Assessment Scale includes a wide range of items relating to gross motor function. It is unlikely that such a scale would detect functional improvements relating to a small area such as the hand or foot. These methodological inadequacies increase the chance of reported effects being the product of measurement bias. Finally, the ability of this review to draw conclusions and formulate recommendations regarding the use of sensory training in stroke rehabilitation is hampered by the diverse range of interventions, outcome measures and subject characteristics included across the available literature. As in all clinical studies, homogeneity of patients, interventions and outcome measures were difficult to obtain. However, this systematic review provides an overview of the existing research on sensory training and provides a basis for future research to improve upon the current knowledge base.

Implications for clinical practice Despite strong neurophysiological evidence demonstrating the importance of afferent input in driving cortical reorganization, a paucity of high-quality research exists examining the link between sensory training and functional improvements in those with stroke. However, the results of this meta-analysis suggest there is some evidence to support the use of passive sensory training to

Retraining of sensation after stroke Based on these findings, there is limited evidence for the use of active sensory training protocols to produce improvements in function, cutaneous sensation or proprioception in the clinical setting. Passive sensory training may serve as a useful adjunct to standard rehabilitation protocols when the clinician aims to improve hand function and dexterity. Passive sensory training using electrical stimulation has a high degree of clinical utility. The majority of rehabilitation departments have access to electrical stimulation devices such as the portable transcutaneous electrical nerve stimulation (TENS) unit. There are relatively few risks associated with electrical stimulation treatments and these are easily screened for prior to commencing treatment. While the optimal stimulation parameters are yet to be determined, the results of this systematic review suggest that electrical stimulation delivered at low frequencies (10 Hz) and at intensities sufficient to evoke strong paresthesias in the target tissue is effective in improving hand dexterity following stroke. Furthermore, these improvements were obtained following relatively short training durations. These factors make passive sensory training a feasible option in the current rehabilitation setting.

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Conclusion
Moderate evidence exists to support the use of passive sensory training to improve hand function and dexterity following stroke. The results of active sensory training protocols are less convincing, although at face value a number of individual studies report positive effects on function, cutaneous sensation and proprioception. Further high-quality research is needed to determine the effects of both passive and active sensory training paradigms post stroke. In addition, research evaluating the most effective training durations and intervention parameters is needed to inform clinical recommendations. Clinical messages  Passive sensory training may assist in improving hand function and dexterity following stroke.  Evidence for active sensory training is limited by small sample sizes, subject heterogeneity and unreliable outcome measures.  Further high-quality research is required to determine the effectiveness of sensory training in stroke rehabilitation.

Implications for research While sensory training has been advocated as a method to produce improvements in impairment and function in those post stroke, the lack of high-quality research in this area prevents the formation of sound recommendations for clinical practice. Future research should focus on highquality randomized controlled trials with high statistical power and consistent and reliable outcome measures. Assessment of the optimal protocols for inducing functional change with respect to both cutaneous electrical stimulation and active sensory training tasks is also necessary before standardized treatment strategies can be developed. However, the large number of stroke patients who suffer from sensory deficits coupled with the positive benefits of sensory training identified in this review indicate that further research into this area is certainly warranted.

Acknowledgements SM Schabrun is supported by an Australian Postgraduate Award and a Healthy Ageing Research Cluster scholarship from the University of Adelaide. Statement of conflict of interest None of the authors have any conflict of interest in the submission of this manuscript. All authors made a significant contribution to the inception, data collection, analyses and writing of this work.

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Appendix 1 Search strategy for the MEDLINE database Search terms Population Stroke Cerebrovascular Accident CVA Hemiplegi$ Cutaneous stimulation Electrical stimulation Afferent stimulation Sensory stimulation Somatosensory stimulation Sensory training Sensory retraining Sensory education Sensory re-education Sensory rehabilitation OR AND one of the following OR Combination

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Passive sensory training

Active sensory training

OR

Search limited to articles published in the English language. Truncated search terms were used where possible.

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