Introduction
Stroke is a leading cause of disability in the United States (Verani et al, 2021). Persistent impairment of sensory and motor function of the upper extremity following a stroke is common, resulting in reduced functional independence (Stewart & Cramer, 2013). Current clinical practice in occupational therapy for neurorehabilitation may focus on compensatory methods that enhance daily activities. However, advancements in neuroscience have allowed for a nuanced understanding of neural mechanisms unveiling new opportunities for treatment approaches in rehabilitation. (Pomeroy et al., 2011).
Recovery after stroke is enhanced by neuroplasticity, or the reorganization of neural networks promoting the re-acquisition of motor skills (Nudo, 2013). Interventions designed to facilitate cortical reorganization, such as constraint induced movement therapy (CIMT), are documented in the literature (Wolf et al., 2006). Recently, adjuvant therapies that modulate the central nervous system have been examined. These techniques are known as priming and are delivered prior to or concurrent with an intervention. The purpose of priming is to initiate a neural and behavioral change (Stoykov & Madhavan, 2015). There are various priming paradigms that leverage neural mechanisms including: stimulation-based priming; motor imagery and action observation; sensory-based priming; movement-based priming; and pharmacology-based priming. See Stoykov & Madhavan (2015) for review.
Several reviews have examined the effectiveness of priming in neurorehabilitation but particularly focusing on stimulation-based and movement-based priming (Bolognini et al., 2009; Stoykov et al., 2017; Stoykov & Madhavan, 2015). A limited amount of research focuses on the effectiveness of sensory-based priming for the post-stroke population. Sensory-based priming is the modulation of sensory input via sensory stimulation or a sensory deprivation paradigm. Sensory-based priming techniques can alter the organization of the somatosensory cortex (Ridding, McKay, Thompson, & Miles, 2001) and improve motor outcomes (Conforto et al, 2010). This is possible due to the close connection between the primary sensory cortex and motor cortex (Catani et al., 2017). Sensory stimulation is implemented via peripheral nerve stimulation (PNS), somatosensory electrical stimulation (SES), or muscle vibration. PNS is the application of electrical stimulation to the skin overlying peripheral nerves via electrodes, whereas SES is the more general application of electrical stimulation to the upper extremity (Conforto et al., 2010). Stimulation occurs below the motor threshold, thus not evoking a motor output. Muscle vibration occurs via mechanical oscillation, transferring energy from a mechanical device to the surface of the skin and is applied either focally or to the whole body (Rittweger, 2010). Temporary functional deafferentation (TFD), a form of sensory deprivation, involves reducing sensory input from an area adjacent to the targeted effector to reorganize sensory cortex. TFD may be targeted to the ipsilesional or contralesional cortex and can be implemented using various methods such as an anesthetic cream or a tourniquet (Floel et al., 2004; Sens et al., 2012).
Sensory priming is cost-effective, safe, and easy to implement in the clinic. However, an improved understanding of the existing evidence is required to effectively employ such interventions and move the field forward. To address this need, we asked the following research question: does sensory-based priming, in combination with a motor-based intervention, result in improved upper extremity motor function in adult persons with stroke? Due to the variety of modalities associated with sensory-based priming, we concluded that a scoping review would be the optimal method to address our research question.
It is notable that there is considerable research on post-stroke sensory training, a skill-based intervention technique that includes using specific, graded, sensory discrimination tasks, attentive exploration of stimuli with vision occluded, deliberate anticipation, quantitative feedback, and stimulus generalization (Carey & Matyas, 2005;). The purpose of sensory training is for post-stroke individuals to relearn skills identifying sensory features of objects during manipulation. The purpose of sensory priming, however, is to manipulate cortical input and facilitate an increased motor response that forms the basis for this review.
Methods
This scoping review followed the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) statement and recommendations from the Cochrane collaboration (Higgins et al., n.d.; Moher et al., 2015).
Data Sources and Search Strategy
After consultation with a librarian, a literature search in the following electronic databases was conducted: PubMed, CINAHL, Web of Science, and Embase. The MeSH database identified terms to maximize results. Search terms were grouped using ‘OR’ to yield a broad list of possible articles (Table 1). The authors also completed a manual search of key authors and systematic reviews to assure inclusion of all relevant articles.
Table 1.
Search terms by database.
| Database | Search terms |
|---|---|
| PubMed | ("Sensory priming" OR “priming” OR "Sensory deafferentation" OR "Sensory stimulation" OR "vibration" OR “vibratory” OR "temporary functional deafferentation" OR “bier block” OR "remote limb ischemic conditioning" OR "peripheral nerve stimulation" OR "mesh glove" OR "cutaneous stimulation" OR "somatosensory stimulation" OR “sensory deprivation” OR (“electrical stimulation” AND “priming”)) AND (stroke* OR stroke[mesh]) NOT (animals[mesh] NOT humans[mesh]) |
| Web of Science | ("Sensory priming" OR “priming” OR "Sensory deafferentation" OR “deafferentation” OR "Sensory stimulation" OR "vibration" OR “vibratory” OR "temporary functional deafferentation" OR “peripheral nerve stimulation" OR "mesh glove" OR "cutaneous stimulation" OR "somatosensory stimulation" OR “sensory deprivation” OR (“electrical stimulation” AND “priming”)) AND (stroke*) |
| Embase | ("Sensory priming" OR “priming” OR "Sensory deafferentation" OR “deafferentation” OR "Sensory stimulation" OR "vibration" OR “vibratory” OR "temporary functional deafferentation" OR “bier block” OR "remote limb ischemic conditioning" OR "peripheral nerve stimulation" OR "mesh glove" OR "cutaneous stimulation" OR "somatosensory stimulation" OR “sensory deprivation” OR (“electrical stimulation” AND “priming”)) AND (stroke*) NOT ([animals]/lim NOT [humans]/lim) |
| CINAHL | ("Sensory priming" OR “priming” OR "Sensory deafferentation" OR “deafferentation” OR "Sensory stimulation" OR "vibration" OR “vibratory” OR "temporary functional deafferentation" OR “bier block” OR "remote limb ischemic conditioning" OR "peripheral nerve stimulation" OR "mesh glove" OR "cutaneous stimulation" OR "somatosensory stimulation" OR “sensory deprivation” OR (“electrical stimulation” AND “priming”)) AND (stroke OR (MH “stroke”)) NOT (MH "Animals" NOT MH "Human") |
Eligibility Criteria
The initial search included research studies of any format and study design though systematic reviews and citations without full text availability were later excluded. The authors included articles that assessed sensory-based priming per the previous definition. To meet the definition of sensory-based priming, the priming activity must have occurred immediately prior to or concurrent with a primary intervention. Additional article criteria included: (1) human adult participants at any phase of post-stroke rehabilitation, (2) use of a behavioral outcome measure, (3) published in English, and (4) published in or after 2010. Excluded studies include: (1) animal studies, (2) studies with other populations (3) studies that assessed a priming paradigm other than sensory-based; (4) studies that did not include statistical analyses; or (5) studies without a motor-based intervention.
Selection Process
Figure 1 depicts the article selection process based on PRISMA guidelines (Moher et al., 2015). (See Supplemental Figure 1). The initial search yielded 2,540 articles (1,678 articles after removing duplicates). Four reviewers performed an initial screening of titles and abstracts, considering the eligibility criteria. The reviewers divided the 1,678 articles in half by alphabetical order of titles, and two pairs of reviewers screened each half. An initial comparison yielded an inter-rater reliability (using Cohen’s Kappa Coefficient) of 84.2% for the first pair of reviewers and 84.9% for the second pair of reviewers. After the initial screening, 218 articles were identified for full-text screening. Each of the reviewers were assigned a quarter of the remaining articles, with a second reviewer assigned to double-check each final list. When a disagreement between two reviewers occurred, all reviewers discussed until a consensus was reached.
Figure 1.

PRISMA Flow Chart, From: Moher D, Liberati A, Tetzlaff J, Altman DG, The PRISMA Group (2009). Preferred Reporting Items for Systematic Reviews and Meta-Analyses: The PRISMA Statement. PLoS Med 6(6): e1000097. doi:10.1371/journal.pmed1000097
For more information, visit www.prisma-statement.org
Reasons for article exclusion during full-text screening include: (1) failing to meet the definition of sensory-based priming (n = 82); (2) the article was classified as a review or protocol paper (n = 78); (3) only healthy participants included (n = 16); (4) use of animal model (n = 1); and (5) no intervention for the upper extremity (n = 5). Additionally, articles were removed if the priming was paired with an intervention in a way that prevented clear interpretation of the results of priming (n = 1) or if there were no relevant outcome measures (n = 5). The final list reviewed and approved by all four reviewers, included 30 articles.
Data Items and Data Extraction Process
A standardized charting form was developed to capture the following descriptive data: study details (type of study, year, and country), objective, design, participants, intervention, type of priming, parameters of priming, outcomes, WHO International Classification of Functioning, Disability and Health (ICF) level of outcomes, and results. The PICO (Patient Problem or Population, Intervention, Comparison or Control, and Outcome) framework was used to capture study details.
Results
Description of studies
The articles in this review are inclusive of various study designs, including 20 randomized controlled trials, eight quasi-experimental studies, and two single-subject design studies. Articles include pilot studies, feasibility studies, and proof-of-concept designs. Blinding protocols varied among studies, with two studies classified as triple-blind, 13 double blind, 10 single blind, and five that did not report on blinding. The chronicity of studies was various; nineteen studies included only participants more than six months post-stroke (chronic), five included participants less than six months post (subacute), one included only participants who were one week or less post-stroke (acute), and five included a range of chronicity. Studies varied in duration from one day to 12 weeks, with the total number of sessions ranging from one session to 70 sessions. All selected studies performed a baseline and post-intervention test, and 12 studies included a follow-up evaluation. A detailed summary of the characteristics of included studies are in Table 2.
Table 2.
Study Characteristics
| Priming type |
First author, year | Study design; Blinding | Sample size total, E, C |
Mean age | Chronicity | Length of study |
|---|---|---|---|---|---|---|
| PNS/SES | Carrico et al., 2016a | RCT two-group parallel; double-blind | 19 E: 10 C: 9 |
- E: 56.7 C: 54.56 |
Chronic | 10 consecutive days |
| Carrico et al., 2016b | RCT two-group parallel; double-blind | 36 E: 18 C: 18 |
- E: 58.7 C: 65.4 |
Chronic | 10 consecutive days | |
| Carrico et al., 2018 | RCT two-group parallel study; double-blind | 55 E: 33 C: 22 |
- 58 63 |
Chronic | 6 weeks | |
| Conforto et al., 2010 | QE two-group parallel; double-blind | 22 SUB: 11 SUP: 11 |
- SUB: 59.3 SUP: 64.2 |
Subacute | 4 weeks | |
| dos Santos-Fontes et al., 2013 | RCT two-group parallel pilot; double-blind | 20 E: 10 C: 10 |
- E: 52.2 C: 59.1 |
Chronic | 4 weeks | |
| Fleming et al., 2015 | RCT two-group parallel; double-blind | 33 E: 16 C: 17 |
61.5 E: 62.3 C: 60.6 |
Subacute, Chronic | 4 weeks | |
| Ghaziani et al., 2018 | RCT two-group parallel; single-blind | 102 E: 53 C: 49 |
- E: 72 C: 71 |
Acute | 2 weeks | |
| Ikuno et al., 2012 | RCT - crossover pilot; no blinding | 22 IM: 11 DE: 11 |
- IM: 68.8 DE: 70.1 |
Subacute | 2 weeks | |
| Lee et al., 2015 | RCT multi-arm parallel; single-blind | 48 MT + MG: 15 MT: 17 MT + S: 16 |
- MT+MG: 52.50 MT: 56.64 MT+S: 49.10 |
Chronic | 4 weeks | |
| Lin, Chen et al., 2014 | RCT two-group parallel pilot; single-blind | 16 E: 8 C:8 |
55.64 E: 56.31 C: 54.97 |
Chronic | 4 weeks | |
| Lin, Huang et al., 2014 | RCT multi-arm parallel; single-blind | 43 MT + MG: 14 MT: 14 C: 15 |
- MT+MG: 55.79 MT: 56.01 C: 53.34 |
Chronic | 4 weeks | |
| Miyasaka et al., 2016 | RCT two-group parallel; no blinding | 30 E: 15 C: 15 |
- E: 56.9 C: 64.9 |
Subacute | 2 weeks | |
| Pan et al., 2018 | RCT two-group parallel; single-blind | 12 E: 6 C: 6 |
56.5 E: 54.5 C: 58.5 |
Subacute, Chronic | 8 weeks | |
| Stein et al., 2010 c | RCT two-group parallel pilot; triple-blind | 30 E: 15 C: 15 |
- E: 60.8 C: 66.0 |
Chronic | 4 weeks | |
| Sullivan et al., 2012 | QE two-group parallel; double-blind | 38 E: 20 C:18 |
60.6 E: 61.6 C: 59.5 |
Chronic | 4 weeks | |
| Sullivan et al., 2015 | QE one-group pilot study; no blinding | 11 | 59.36 | Chronic | 5 weeks | |
| Vibration | Ahn et al., 2019 | RCT two group parallel; single-blind | 60 WBV: 30 ULC: 30 |
- WBV: 58.7 ULC: 60.7 |
Subacute | 4 weeks |
| Boo et al., 2016 | QE one-group; no blinding | E: 14 | E: 50.4 | Chronic | 8 weeks | |
| Calabro et al., 2017 | RCT two-group parallel pilot; double-blinding | 20 E: 10 C: 10 |
- E: 66 C: 67 |
Subacute, Chronic | 8 weeks | |
| Constantino et al., 2014 | QE one-group pilot; single-blind | E: 16 | E: 61.69 | Chronic | 4 weeks | |
| Dang et al., 2019 | RCT two-group parallel; double-blind | 95 E1: 32 E2: 33 C: 30 |
59.5 E1: 57.8 E2: 60.6 C: 60.0 |
Acute, Subacute, Chronic | 4 weeks | |
| Law et al., 2018 d | QE two-group parallel pilot; no blinding | 12 E: 6 C: 6 |
67.17 E: 65.5 C: 68.83 |
Subacute | 12 weeks | |
| Lee et al., 2016 | RCT multi-arm parallel pilot; double-blind | 45 WBV + TRT: 15 WBV: 15 C: 15 |
- WBV + TRT: 58.53 WBV: 59.20 C: 60.24 |
Chronic | 4 weeks | |
| Marconi et al., 2011 | RCT two-group parallel; double-blind | 30 E: 15 C: 15 |
65.0 E: 63.6 C: 66.3 |
Chronic | 3 days | |
| Seo et al., 2014 | Single-subject pilot; single-blind | 10 | 63.4a | Chronic | 1 day | |
| Seo et al., 2019 | RCT two-group parallel pilot; triple-blind | 12 E: 6 C: 6 |
- E: 61 C: 64 |
Subacute, Chronic | 2 weeks | |
| Stein et al., 2010 c | ||||||
| TFD | Sens et al., 2012 | QE two-group crossover; single-blind | 36 | 58.06 | Chronic | 2 days |
| Sens et al., 2013 | QE two-group parallel; no blinding | 66 E: 46 C: 20 |
- E: 55.04 C: 55.7 |
Chronic | 1 day | |
| Weiss et al., 2011 | Single-subject (one-group) crossover; double-blind | 16 | 53.63 | Chronic | 2 days |
Note: Abbreviations: PNS=peripheral nerve stimulation, SES=somatosensory electrical stimulation, E=experimental group, C=control group, SD=standard deviation, M=male, F=female, RCT=randomized controlled trial, QE=quasi-experimental, SUB=subsensory, SUP=suprasensory, Q=quartile, IM=immediate, DE=delayed, MT=mirror therapy, MG=mesh glove, S=sham, WBV=whole-body vibration, ULC=upper and lower cycle, TRT=task-related training, TFD=temporary functional deafferentation
Mean calculated manually using existing data
Reported by original authors as a percentage of sample
Study is cross-referenced under two subtypes of sensory-based priming: PNS and vibration
This study also included thermal stimulation
Outcome measures
Thirty outcome measures are identified as either primary or secondary outcomes in the 30 studies. The measures are categorized according to the ICF with 13 of the 25 measures classified under body functions and structures domain and nine measures classified under activities domain. The most common assessment tool used in the body functions and structure domain was the Fugl-Meyer Assessment of Motor Recovery (FMUE), identified in 16 (53.3%) of the 30 included studies (Fugl-Meyer et al., 1975). Within the activities domain, the Wolf-Motor Function Test (WMFT) was the most frequently used assessment in nine studies (30%) (Wolf et al., 2001). Varieties of sensory outcome measures are in nine of the 30 included studies (30%). A list of all motor and sensory-based outcome measures are in Table 3.
Table 3.
Outcome Measures and Individual Study Results
| Priming category |
First author, year |
Evaluation measurements |
Motor and sensory outcome measures |
Main results (Between-group differences) |
|---|---|---|---|---|
| PNS/SES | Carrico et al., 2016a | Baseline, EOT, 1-month FU | FMA; ARAT; WMFT | SS improvements at EOT for the WMFT (timed and lift portions only), ARAT and FMA (p< .05). Improvements remained at FU for ARAT and WMFT (p< .05). |
| Carrico et al., 2016b. | Baseline, EOT, 1-month FU | FMA; ARAT; WMFT | SS improvements in all outcome measures at EOT and FU (p < .05). | |
| Carrico et al., 2018 | Baseline, EOT, 1-month FU, 4-month FU | FMA; ARAT; WMFT | No SS improvement for the FMA. SS improvements at EOT for WMFT and ARAT (p < .05). Improvements remained at both FU’s for ARAT (p < .05). | |
| Conforto et al., 2010 | Baseline, EOT, 2-3 month FU | JTHFT; FIM; Pinch | SS improvements on the JTHFT for the SUB group at EOT (p< .05), but not at FU. No SS improvements for the FIM or pinch. | |
| Dos Santos-Fontes, et al., 2013 | Baseline, EOT, 4-month FU | JTHFT | SS improvements in the JTHFT at EOT and FU (p < .05). | |
| Fleming et al., 2015 | Baseline x2 (1 week apart), EOT, 3-month FU, 6-month FU | FMA; ARAT | No SS improvements on the FMA. SS improvements at EOT (p < .05), but not at FU for the ARAT. | |
| Ghaziani et al., 2018 | Baseline, EOT, 6-month FU | FMA; Perceptual Threshold of Touch; Grip; Pinch; BBT | No SS between-group difference for any outcome measure. | |
| Ikuno et al., 2012 | Baseline, one week, EOT | Grip; Pinch; WMFT; BBT | No SS between-group difference for any outcome measure. | |
| Lee et al., 2015 | Baseline and EOT | FMA ;NSA; Muscle tone/stiffness (Myoton); BBT; FIM | No SS improvements for the FMA or NSA. For the BBT, the MT+MG and MT+S improved (p < .05) more than the MT group. For the FIM, MT+MG and MT+S had SS improvements compared to MT group (p < .05). For Muscle tone/stiffness (Myoton), the extensor digitorum and flexor carpi radialis tone had significant improvements in the MT+MG group (p < .05). | |
| Lin, Chen et al., 2014 | Baseline, EOT | MAS; ARAT; BBT; | SS improvements at EOT for the ARAT and BBT for MT + MG in comparison to MT alone. No significant between-group difference for the MAS. | |
| Lin, Huang et al., 2014 | Baseline, EOT | FMA; Muscle tone/stiffness (Myoton); BBT; Abilhand | SS improvements in FMUE for MT+MG and MT alone compared to control. SS improvements in BBT for MT+MG compared to MT alone. | |
| Miyasaka et al., 2016 | Baseline, EOT | FMA; AROM | No SS between groups difference for the FMA. SS improvements in shoulder AROM at EOT (p < .05). | |
| Pan et al., 2018 | Baseline, 4 weeks, EOT, 1-month FU | FMA | No SS between-groups difference. | |
| Stein et al., 2010 c | Baseline, EOT, 1-month FU | FMA; Semmes-Weinstein Monofilament; RPS; MAS; ARAT; WMFT | No SS between-group differences for changes scores on any of the outcome measures. | |
| Sullivan et al., 2012 | Baseline, EOT | FMA; NSA; PTTES; Tardieu Spasticity; AMAT | No SS between-group differences for changes scores on any of the outcome measures. | |
| Sullivan et al., 2015 | Baseline, EOT, 3-month FU | NSA; STREAM-UE; JTHFT | SS between-group improvements for the NSA and JTHFT at EOT and FU (p < .05). No significant improvements found for the STREAM-UE. | |
| Vibration | Ahn et al., 2019 | Baseline, EOT | Grip; MFT | SS improvements bin the WBV group for the MFT and for grip (p < .05). |
| Boo et al., 2016 | Baseline, EOT | FMA; MFT; MAS | SS improvements for the majority of participants on the FMA and MFT (p < .05). 6/14 participants had SS improvements on the MAS (p < .05). | |
| Calabro et al., 2017 | Baseline, EOT, 1-month FU | FMA; Kinematic Data (PROM, force, arm weight support); MAS; FIM | SS improvements for all outcome measures at EOT and FU (p < .05). | |
| Constantino et al., 2014 | Baseline, EOT | FMA; Grip; MAS; JTHFT; FIM | SS improvement in all outcome measures (p < .05). | |
| Dang et al., 2019 | Baseline, EOT | FMA; Grip; MAS; WMFT | SS improvements in E1 and E2, with E2 favored for grip and FMA (p < .05). SS improvements in E2 for WMFT (p < .05). SS improvements in E1 and E2 with E1 favored in MAS (p < .05). | |
| Law et al., 2018 d | Baseline, EOT | FMA; MMT; FTHUE-HK | SS improvements at EOT for FMA, MMT and FTHUE-HK (p < .05). | |
| Lee et al., 2016 | Baseline, EOT | FMA; Grip; MAS; WMFT | SS improvements in the WBV+TRT and WBV groups for the FMA (p < .05). SS improvements only in the WBV+TRT group for WMFT, MAS and grip (p < .05). | |
| Marconi et al., 2011 | Baseline, EOT, 1-week post, 2 weeks post FU | MAS; MI-ul; WMFT- FAS | SS improvement for all outcome measures at EOT and FU (p < .05). | |
| Seo et al., 2014 | 4 timepoints (at each block of motor tasks) | Monofilament Test for the thumb and index fingertips; Grip/Pinch; AROM; 9HPT; BBT | SS improvements in the majority of participants for the 9HPT, BBT, and pinch (p < .05). No SS improvements in wrist AROM, grip or monofilament test. | |
| Seo et al., 2019 | Baseline, EOT, 19 days FU | WMFT; BBT | SS improvements for the BBT at EOT and FU (p < .05). No SS improvements in the WMFT. | |
| Stein et al., 2010 c | Baseline, EOT, 1-month FU | FMA; Semmes-Weinstein Monofilament; RPS; MAS; ARAT; WMFT | No SS between-group differences for changes scores on any of the outcome measures. | |
| TFD | Sens et al., 2012 | Baseline, EOT | VFHT; GOT; SSDT | SS improvement on all outcome measures (p < .05). |
| Sens et al, (2013) | Baseline, EOT | VFHT; GOT; SSDT | SS improvement for the VHFT-F, SSDT and GOT (p < .05). No SS improvement for the VHFT-D2. | |
| Weiss et al., 2011 | Baseline, EOT | VFHT; GOT; SSDT | SS improvement on all outcome measures (p < .05). |
Note: Abbreviations: Priming Terms: PNS=peripheral nerve stimulation, SES=somatosensory electrical stimulation, TFD=temporary functional deafferentation, MG=mesh glove, SUB= below sensory detection, WBV=whole-body vibration
Trial Terms: EOT=end of trial, FU=follow-up, E=experimental group, SS=statistically significant, S=sham
Treatment Groups: MT=mirror therapy, TRT=task-related training,
Assessments: FMA= Fugl-Meyer Assessment of Motor Recovery after Stroke, ARAT=Action Research Arm Test, JTHFT=Jepsen-Taylor Hand Function Test, FIM=Functional Independence Measure, BBT=Box and Blocks Test, rNSA=revised Nottingham Sensory Assessment, , MAS= Modified Ashworth Scale, AROM= active range of motion, RPS=Reaching Performance Scale, NSA= Nottingham Assessment of Somato-Sensations, PTTES= Perceptual Threshold of Electrical Stimulation, AMAT= Arm Motor Ability Test, STREAM-UE= Stroke Rehabilitation Assessment of Movement - Upper Extremity, MFT=Manual Function Test, , MMT= manual muscle testing, FTHUE-HK= Functional Test for the Hemiplegic Upper Extremity (Hong Kong version), MI-ul= Motricity Index of the Upper Limb, WMFT=Wolf Motor Function Test, WMFT-FAS= Wolf Motor Function Test-Functional Ability Scale, 9HPT = Nine Hole Peg Test, VFHT= Von Frey Hair Test, GOT= Grating Orienting Task, SSDT= Shape Sorter Drum Task
Data derived from 17/18 participants
Sensory findings were omitted from analysis due to yielding unreliable findings
Study is cross-referenced under two subtypes of sensory-based priming: PNS and vibration
This study also included thermal stimulation
Priming Methods
Three different subtypes of sensory-based priming were included in this review: PNS/SES, vibration, and TFD. Of the 27 studies utilizing sensory stimulation priming methods, there were 16 PNS/SES, 10 vibration, and one that included both PNS/SES and vibration. Specific protocols about dose and stimulation parameters varied. Details are provided in Table 4.
Table 4.
Characteristics of Priming Methods.
| Priming type |
First author, year | Specific priming method | Timing: (prior/concurrent/both) |
Sensory parametersa/ Frequencies |
|---|---|---|---|---|
| PNS/SES | Carrico et al., 2016 | PNS via electrodes | Prior | Suprathreshold |
| Carrico et al., 2016 | PNS via electrodes | Prior | Suprathreshold | |
| Carrico et al., 2018 | SES via electrodes | Prior | Suprathreshold | |
| Conforto et al., 2010 | PNS via electrodes | Prior | Mixed thresholdb | |
| dos Santos-Fontes et al., 2013 | PNS via ReliefBand | Prior | Suprathreshold | |
| Fleming et al., 2015 | SES via electrodes | Prior | Suprathreshold | |
| Ghaziani et al., 2018 | SES via electrodes | Prior | Suprathreshold | |
| Ikuno et al., 2012 | PNS via electrodes | Concurrent | Suprathreshold | |
| Lee et al., 2015 | Mesh Glove | Prior | Suprathreshold | |
| Lin et al., 2014a | Mesh Glove | Concurrent | Mixed thresholdb | |
| Lin et al., 2014b | Mesh Glove | Concurrent | Mixed thresholdb | |
| Miyasaka et al., 2016 | PNS via NMES | Concurrent | Threshold not specified | |
| Pan et al., 2018 | PNS via electrodes | Prior | Suprathreshold | |
| Stein et al., 2010 c | PNS via electrodes | Concurrent | Subthreshold | |
| Sullivan et al., 2012 | Sensory amplitude electrical stimulation via glove electrodes | Concurrent | Suprathreshold | |
| Sullivan et al., 2015 | Sensory amplitude electrical stimulation via glove electrode | Concurrent | Suprathreshold | |
| Vibration | Ahn et al., 2019 | WBV via a Galileo Tilt Table | Prior | Frequency of 4-19 Hz |
| Boo et al., 2016 | WBV via Vibro Wedge | Prior | less than 30 Hz | |
| Calabro et al., 2017 | Vibration via Armeo Power Arm | Concurrent | 80 Hz | |
| Constantino et al., 2014 | Mechano-acoustic vibration via ViSS Device | Concurrent | 300 Hz | |
| Dang et al., 2019 | WBV via Wellengang Vibrator | Prior | 5-15 Hz | |
| Law et al., 2018 d | Muscle vibration via a handheld vibrator | Prior | 91 Hz | |
| Lee et al., 2016 | WBV via a Galileo Tilt Table | Prior | 5-15 Hz | |
| Marconi et al., 2011 | Repeated muscle vibration via CroSystem | Prior | 100 Hz | |
| Seo et al., 2014 | Vibrotactile noise via C-3 tactors | Concurrent | 500 Hz, 60% of sensory threshold | |
| Seo et al., 2019 | Vibration via Therabracelet | Concurrent | 500 Hz, 60% of sensory threshold | |
| Stein et al., 2010 c | Mechanical noise vibration via battery-powered analog signal isolator | Concurrent | 0-100 Hz | |
| TFD | Sens et al., 2012 | TFD via EMLA anesthetic cream | Concurrent | Sensory deprivation |
| Sens et al., 2013 | TFD via EMLA anesthetic cream | Concurrent | Sensory deprivation | |
| Weiss et al., 2011 | TFD via EMLA anesthetic cream | Concurrent | Sensory deprivation |
Abbreviations: PNS=peripheral nerve stimulation, SES=somatosensory electrical stimulation, WBV=whole-body vibration, TFD=temporary functional deafferentation
All parameters were below motor threshold
Via group assignment, one group received subthreshold sensory stimulation while the other received suprathreshold stimulation or the groups received a mix of subthreshold or suprathreshold depending on the individual
Study is cross-referenced under two subtypes of sensory-based priming: PNS and vibration
This study also included thermal stimulation
For PNS/SES, 13 studies applied stimulation via electrodes alone, while others utilized a different conductor as well, including one Relief Band (Woodside Biomedical, Carlsbad, California) and three mesh gloves. Vibration studies included four whole body vibration, three focal vibration, and four mechano-acoustic/white noise vibrations.
Regarding the timing of the sensory stimulation priming, 16 studies (10 PNS/SES and 6 vibration) delivered the priming method prior to the intervention, 10 studies (5 PNS/SES, 4 vibration, and 1 PNS plus vibration) delivered it concurrent with the intervention, and one study delivered PNS/SES both prior to and concurrent with the intervention.
All PNS/SES studies delivered stimulation below the motor threshold level. However the sensory threshold varied and was further differentiated based on amplitude [i.e. sensory stimulation at subthreshold (not detected by participant) or suprathreshold (stimulation was at or above what the participant could detect)]. The majority (11) of PNS/SES studies applied stimulation at threshold or suprathreshold. Three applied subthreshold or suprathreshold sensory parameters according to group assignment. One study did not report specific thresholds used for sensory stimulation. In the vibration studies, four studies used subthreshold stimulation. Three studies used TFD via the application of anesthetic cream to the forearm to block afferent signals to the brain, and the intervention was delivered immediately after application.
Motor training interventions
There were 12 different types of motor training identified in the 30 studies. The interventions utilized include: task-oriented training (n=11); CIMT (n=4); mirror box + functional training (n=2); hand function training (n=1); motor training (n=3); robotics training (n=1); motor training plus self-care practice (n=1); usual care rehabilitation plus practice of the Jebsen-Taylor Hand Function Test (n=2); repetitive exercise (isotonic or isometric) (n=2); arm training not specified (n=1); occupational therapy (n=1); and a combination of mobilization, stretching and facilitation (n=1). Treatment protocols varied between studies. Overall, the total number of minutes of primary intervention time ranged from 25 minutes to 4,320 minutes across the 30 studies. A detailed description of the primary intervention characteristics is provided in Table 5.
Table 5.
Characteristics of Motor Training Interventions
| Priming type |
Citation | Type of motor training | Specific sub- task duration |
Total primary intervention duration |
Total number of sessions |
Total Intervention timea |
|---|---|---|---|---|---|---|
| PNS/SES | Carrico et al., 2016a | Modified CIMT | 216 minutes | 240 minutes (4 hours) | 10 sessions | 2,400 minutes |
| Carrico et al.,, 2016b | High repetition, task-oriented training (TOT) for UE | 4 hours | 4 hours (10 consecutive week days) | 10 sessions | 2,400 minutes | |
| Carrico et al., 2018 | TOT | 4 hours | 4 hours (3x/week 6 weeks) | 18 sessions | 4,320 minutes | |
| Conforto et al., 2010 | JTHFT-related activities and standard rehabilitation | - | - | 12 sessions | - | |
| Dos Santos-Fontes et al., 2013 | Home-based motor training using JTHFT-related tasks | 3 minutes | 15 minutes (7x/week for 4 weeks) | 28 sessions | 420 minutes | |
| Fleming et al., 2015 | TOT | 30 minutes | 30 minutes (3x/week for 4 weeks) | 12 sessions | 360 minutes | |
| Ghaziani et al., 2018 | Arm training with active, repetitive task practice | 15 minutes | 15 minutes (Daily during course of hospital stay for 4 weeks maximum) | Variable based on hospital length of stay (average 12-13 total sessions) | E (Median): 15.7 hours; C (Median): 10.1 hours | |
| Ikuno et al., 2012 | TOT | 10 minutes/task with 2 minute rest breaks between tasks for 5 tasks total | 1 hour (6 days/week for 2 weeks) | 12 sessions | 720 minutes | |
| Lee et al., 2015 | Mirror therapy & functional task training | 30 minutes mirror therapy and mesh glove stimulation, 30 minutes mirror therapy alone, 30 minutes functional task training alone | 90 minutes (5x/ week for 4 weeks) | 20 sessions | 1,800 minutes | |
| Lin et al., 2014a | Mirror box training & functional training | Warm Up: 10 minutes, MT: 1 hour; FT: 20 minutes | 90 minutes (5x/ week for 4 weeks) | 20 sessions | 1,800 minutes | |
| Lin et al., 2014b | Mirror box & functional training | Warm-up: 10 minutes; MT: 1 hour, Task practice: 20 minutes | 90 minutes (5x/week for 4 weeks) | 20 sessions | 1,800 minutes | |
| Miyasaka et al., 2016 | Robot-based arm training in horizontal plane | 60 minutes | 60 minutes (5x/ week for 2 weeks) | 10 sessions | 600 minutes | |
| Pan et al., 2018 | Routine hand training using functional tasks | 20 minutes | 20 minutes (2x/ week for 8 weeks) | 16 sessions | 320 minutes | |
| Stein et al., 2010 b | TOT using client-specific activities | 1 hour | 1 hour (3x/week for 4 weeks with 1 initial visit) | 13 sessions | 780 minutes | |
| Sullivan et al., 2012 | Home-based TOT using COPM-identified activities | 30 minutes | 30 minutes (2x daily, 5x/week for 4 weeks) | 40 sessions | 1,200 minutes | |
| Sullivan et al., 2015 | Home-based TOT | 30 minutes-1 hour | 30 minutes (2x daily, 5 days/week for 5 weeks) with two supervised sessions lasting 1 hour | 50 sessions (+ at least 2 supervised sessions in clinic) | 1,500 minutes | |
| Vibration | Ahn et al., 2019 | TOT of ADLs | 30 minutes | 30 minutes (5x/week for 4 weeks) | 20 sessions | 600 minutes |
| Boo et al., 2016 | Occupational therapy | 20 minutes | 20 minutes (5x/week for 8 weeks) | 40 sessions | 800 minutes | |
| Calabro et al., 2017 | Repetitive exercises using functional activities to improve UE function | 1 hour | 1 hour (5x/week for 8 weeks) | 40 sessions | 2,400 minutes | |
| Constantino et al., 2014 | Isometric contraction | 30 minutes | 30 minutes (3x/week for 4 weeks) | 12 sessions | 360 minutes | |
| Dang et al., 2019 | TOT | 15 minutes | 15 minutes (5x/week for 4 weeks) | 20 sessions | 300 minutes | |
| Law et al., 2018 d | Motor training and self-care training | Motor training: 15 minutes; Self-care training: 30 minutes | 45 minutes (2x/week for 12 weeks) | 24 sessions | 1,080 minutes | |
| Lee et al., 2016 | Task-related training | 30 minutes | 30 minutes (3x/week for 4weeks) | 12 sessions | 360 minutes | |
| Marconi et al., 2011 | Physiotherapy including passive/active mobilization, neuromuscular facilitation, and stretching | 60 minutes | 60 minutes (3x/week for 1 week) | 3 sessions | 180 minutes | |
| Seo et al., 2014 | Repetitive practice of motor tasks including 9-HPT, BBT and pinch | All tasks repeated 4 times with 2 minute breaks between each and 5 minutes breaks between blocks | - | 1 session | - | |
| Seo et al., 2019 | TOT of fine motor and dexterity-focused activities | 10 minutes for tasks from 11 different movement groups | 2 hours (3x/week for 2 weeks) | 6 sessions | 720 minutes | |
| Stein et al., 2010 b | ||||||
| TFD | Sens et al., 2012 | CIMT | 3.5 hours | 3.5 hours (2x/week for 1 week) | 2 sessions | 540 minutes |
| Sens et al., 2013 | CIMT | 3.5 hours | 3.5 hours | 1 session | 210 minutes | |
| Weiss et al. 2011 | CIMT | Supervised motor practice: 3.5 hours; Unsupervised homework activities: 3.5 hours | Waking hours for 2 consecutive days | 2 sessions | - |
Abbreviations: PNS=peripheral nerve stimulation, SES=somatosensory electrical stimulation, CIMT=Constraint Induced Movement Therapy, UE=upper extremity, TOT=task-oriented training, JTHFT=Jepsen Taylor Hand Function Test, E=experimental group, MT=mirror therapy, FT=functional training, FES=functional electrical stimulation, COPM=Canadian Occupational Performance Measure, ADLs=activities of daily living, 9-HP=9 Hole Peg Test, BBT=Box and Block Test, TFD=temporary functional deafferentation
Information calculated manually using existing data
Study is cross-referenced under two subtypes of sensory-based priming: PNS and vibration
Total minutes was calculated assuming 100% compliance for all subjects
This study also included thermal stimulation
Study Outcomes
Of the 30 studies included, 23 studies reported statistically significant improvements (referred to as “significant” from this point on) in at least one motor or sensory-based outcome for the primed participants, while seven studies reported no significant improvements.
PNS/SES
Of the 16 studies that used PNS or SES as a sensory priming method, 10 studies reported a significant between-group difference favoring the primed group in at least one motor and/or sensory outcome measure. Five of the 16 studies that used body functions and structures measures and 10 of the 14 studies that used outcomes classified under the activities domain reported significant results.
PNS/SES studies implemented a variety of priming protocols varying from below sensory threshold (subthreshold) to above sensory threshold (suprathreshold). Seven of 12 studies using suprathreshold stimulation reported significant findings. Five studies included subacute participants, and three of those reported significant improvement at post-intervention. Of the 13 studies including only chronic participants, nine reported significant improvement. Ghaziani et al., (2018) included only acute participants and reported no significant results. Of the 10 studies with a follow-up time-point, five reported significant improvement at follow-up.
Vibration
Ten of the 11 vibration studies reported significant improvements favoring the primed group in at least one motor and/or sensory-based outcome measure. Nine out of 10 studies that used body functions and structure outcomes reported positive results, while seven out of nine studies that used activity-based outcome measures also showed positive results. Two of the three studies with subthreshold parameters reported significant improvements. All five studies that included subacute participants or mixed chronicity participants reported significant improvements. Five out of six studies with only chronic participants reported significant improvement. Additionally, three out of the four studies with a follow-up time point had significant follow up results.
TFD
All three studies that used TFD prior to training reported significant between-group differences in favor of the experimental group. The studies reported significant improvements on the SSDT, the von Frey Hair Test, and Grating Orienting Test (Craig, 1999). The studies used chronic participants.
Discussion
Results from this review indicate that sensory-based priming may provide an additive effect to motor training post-stroke. Positive findings were reported for all three sensory-based priming methods, with 10/16 PNS/SES studies, 10/11 vibration studies, and 3/3 TFD studies reporting positive between-group results. The review also points to major obstacles to further analysis in the current literature including: the large variability in dosage of training time (25 to 4,320 minutes); the lack of a follow-up in some of the studies; and the lack of specific guidelines for stimulation parameters.
Influential Factors
Outcome measures
The use of sensory-based priming demonstrated significant improvement at the body functions and structures, and activity levels for PNS/SES, vibration, and TFD protocols. Studies using PNS/SES had the most significant improvements in outcome measures classified under the activity category, such as the Action Research Arm Test or Wolf Motor Function Test (Lyle, 1981; Wolf et al., 2001), implying sensory-based priming using PNS/SES may positively influence a person’s ability to complete functional activities using their affected extremity.
Time Since stroke
Studies with participants at all stages of stroke recovery showed benefit, providing evidence supporting the use of sensory-based priming as a way to facilitate gains through the entire course of stroke recovery.
Presence of a Follow-up Measure
Eight of the 13 studies that included a follow-up time point reported significant improvements that persisted, indicating that the effects of sensory-based priming may exceed the intervention period. These findings are limited due to the relatively few studies with follow-up time points. A previous study reported that motor benefits of somatosensory stimulation persist at least 30 days beyond the final treatment session (Conforto et al., 2007) and this is consistent with the current priming literature (Linder et al., 2019; Stoykov, Corcos, & Madhavan, 2017; Stoykov & Madhavan, 2015). Future studies should incorporate follow-up time points to determine if effects of sensory-based priming persist after training has ceased.
Priming Parameters and Protocols
Stimulation parameters used in the studies were above, at, or below sensory threshold. Suprathreshold parameters were most commonly used (N=24) for vibration, PNS, and SES and yielded positive results in more than half (58.33%) of the studies, indicating that suprathreshold may be the preferred parameter. This is consistent with evidence linking suprathreshold stimulation to changes in neuroplasticity (Ridding et al., 2001). In three studies, PNS/SES was suprathreshold, and the specific intensity was determined based on presence of compound action potentials (Carrico et al., 2016a, Carrico et al., 2016b, Carrico et al., 2018). The suprathreshold and person-specific parameters resulted in both statistically significant changes as well as changes that were in the upper range of the estimated clinically important difference (Page, Fulk, & Boyne, 2012) at both post-test and follow-up for the FMUE (Carrico et al., 2016a, Carrico et al., 2016b). In other studies yielding significant results (Lin et al., 2014a, 2014b), participants received a stimulation protocol specific to the participant’s threshold and score on the Modified Ashworth. This suggests that better outcomes may occur with individually tailored stimulation parameters.
The variety of stimulation parameters used in the various studies emphasizes a current gap in the literature and a significant challenge facing clinicians delivering electrical stimulation, with many therapists deploying stimulation void of evidence-based protocols (Dionne et al., 2020). Future between-group studies are needed comparing stimulation parameters while controlling for other factors such as dosage of training.
The greatest consistency in priming protocols was in the three TFD studies that used anesthetic cream concurrent to CIMT, with significant results reported at post-test. It is possible that the TFD studies yielded comparable positive results due, in part, to the similarities of study design. All three studies utilized CIMT as an intervention for a one to two day timespan, there was no follow-up time point, and outcome measures were identical across studies.
Clinical Implications
This review indicates that sensory-based priming has promise for improving post-stroke recovery. One advantage is that materials required to employ sensory stimulation priming (i.e. tens units, mesh gloves, electrodes and focal vibrators) are relatively inexpensive and accessible in the clinic. Sensory-based priming is a time effective treatment approach as it is applied either prior to or concurrent with intervention. Interventions can easily be client-centered. Finally, this paradigm is relevant to individuals of varying levels of motor impairment, as voluntary movement and physical endurance are not prerequisite skills.
Limitations
The current review aimed to capture a wide breadth of current evidence regarding sensory-priming for stroke rehabilitation. Inclusion and exclusion criteria for articles were set to include a range of study designs, treatment protocols, outcome measures, and participant characteristics. This review was inclusive of studies that did not include control groups. Some studies included in this review were pilot or feasibility studies that yielded small sample sizes and larger sample sizes would ensure the generalizability of findings. Finally, the review is limited by publication bias.
Conclusion
Sensory-based priming may prove an effective remedial approach to stroke rehabilitation. The review highlights preliminary support for sensory-based priming to improve outcomes. It also points to a lack of consistency in protocols, parameters, outcome measures, priming delivery methods, and sample sizes. Future studies could identify the most efficient protocols and stimulation parameters.
Acknowledgements:
1R01HD091492-03; 2R01HD075777-06A1
Footnotes
Conflict of interest: The authors have no conflicts of interest.
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