SHS EMG Biofeedback

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TYPE Systematic Review

PUBLISHED 10 January 2023


DOI 10.3389/fneur.2022.1056156

EMG biofeedback combined


OPEN ACCESS with rehabilitation training may
be the best physical therapy for
EDITED BY
Jingling Chang,
Beijing University of Chinese
Medicine, China

REVIEWED BY
improving upper limb motor
Jacopo Lanzone,
Sant’Isidoro Hospital Ferb Onlus
Trescore Balneario, Italy
function and relieving pain in
Carmen Parra-Farinas,
University of Toronto, Canada patients with the post-stroke
shoulder-hand syndrome: A
*CORRESPONDENCE
LiHua Gu
kmglh169@163.com
SPECIALTY SECTION
This article was submitted to
Bayesian network meta-analysis
Neurorehabilitation,
a section of the journal
Frontiers in Neurology Sisi Feng1 , Mingzhi Tang1 , Gan Huang1 , JuMei Wang1 ,
RECEIVED 28 September 2022 Sijin He2 , Duo Liu2 and LiHua Gu2*
ACCEPTED 13 December 2022
PUBLISHED 10 January 2023 1
Yunnan University of Traditional Chinese Medicine, Kunming, China, 2 Department of Rehabilitation,
CITATION
Kunming Hospital of Traditional Chinese Medicine, The Third Affiliated Hospital of Yunnan University
Feng S, Tang M, Huang G, Wang J, of Chinese Medicine, Kunming, China
He S, Liu D and Gu L (2023) EMG
biofeedback combined with
rehabilitation training may be the best Background: Post-stroke shoulder-hand syndrome (SHS), although not a
physical therapy for improving upper
limb motor function and relieving pain life-threatening condition, may be the most distressing and disabling problem
in patients with the post-stroke for stroke survivors. Thus, it is essential to identify effective treatment
shoulder-hand syndrome: A Bayesian
strategies. Physical therapy is used as a first-line option for treating SHS;
network meta-analysis.
Front. Neurol. 13:1056156. however, it is unclear which treatment option is preferred, which creates
doi: 10.3389/fneur.2022.1056156 confusion in guiding clinical practice. Our study aims to guide clinical
COPYRIGHT treatment by identifying the most effective physical therapy interventions for
© 2023 Feng, Tang, Huang, Wang, He,
improving clinical symptoms in patients with post-stroke SHS using Bayesian
Liu and Gu. This is an open-access
article distributed under the terms of network meta-analysis.
the Creative Commons Attribution
License (CC BY). The use, distribution
Methods: We conducted a systematic and comprehensive search of data from
or reproduction in other forums is randomized controlled trials using physical therapy in patients with SHS from
permitted, provided the original database inception to 1 July 2022. Fugl-Meyer Upper Extremity Motor Function
author(s) and the copyright owner(s)
are credited and that the original Scale (FMA-UE) and pain visual analog score (VAS) were used as primary
publication in this journal is cited, in and secondary outcome indicators. R (version 4.1.3) and STATA (version 16.0)
accordance with accepted academic
practice. No use, distribution or
software were used to analyze the data.
reproduction is permitted which does Results: A total of 45 RCTs with 3,379 subjects were included, and the
not comply with these terms.
intervention efficacy of 7 physical factor therapies (PFT) combined with
rehabilitation training (RT) was explored. Compared with the control group,
all the PFT + RT included were of statistical benefit in improving limb motor
function and pain relief. Also, our study indicated that EMG biofeedback
combined with RT (BFT + RT) [the surface under the cumulative ranking curve
(SUCRA) = 96.8%] might be the best choice for patients with post-stroke SHS.
Conclusion: EMG biofeedback combined with rehabilitation training may be
the best physical therapy for improving upper limb motor function and relieving

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Feng et al. 10.3389/fneur.2022.1056156

pain in patients with post-stroke SHS according to our Bayesian network


meta-analysis results. However, the above conclusions need further analysis
and validation by more high-quality RCTs.
Systematic review registration: www.crd.york.ac.uk/prospero/, identifier:
CRD42022348743.

KEYWORDS

stroke, shoulder-hand syndrome (SHS), physical therapy, rehabilitation training,


network meta analyses

Introduction stellate nerve block, steroid hormone joint cavity injection


closure, intravenous bisphosphonate injection, intradermal
Shoulder-hand syndrome (SHS), also known as reflex injection of botulinum toxin, and other invasive drugs (8–11).
sympathetic dystrophy (RSD), is mainly characterized by While pharmacological treatment is convenient and quick,
local pain, limitation of upper extremity movement with its long-term use will produce side effects such as infection,
swelling, abnormal skin temperature, and skin changes. As poor compliance, and drug resistance. Consequently, it can
a common complication in stroke patients with hemiplegia, only relieve some clinical symptoms but cannot fundamentally
usually occurring in patients within 1–3 months after stroke, control and treat the occurrence and development of SHS (12).
SHS is a crucial factor affecting the recovery of motor function The treatment guidelines (13) highlight that since pain and
in the upper extremity of patients (1, 2). Nonetheless, failure limb dysfunction are the main clinical problems associated
to provide timely and unreasonable interventions may prolong with SHS, early physical therapy intervention is the basis and
SHS patients’ recovery, even resulting in permanent deformities first-line choice for SHS treatment. In addition, most experts,
of the shoulder, upper limb, and finger, which may seriously even those who use more invasive interventional techniques,
affect their daily lives and prognoses (3). agree that effective treatment should emphasize functionally
Modern medicine has not yet elucidated the pathogenesis of focused interventions, particularly physical therapy that aims
SHS after stroke. It may be related to reflex sympathetic nerve at normalizing the function of the affected limb and alleviating
damage that leads to a series of inflammatory and autoimmune problems associated with disuse (14).
reactions, and the generation of abnormal cytokines (4). Physical therapy, as the main body of rehabilitation
Furthermore, limb paralysis impairs the circulation of body treatment, includes exercise therapy based on rehabilitation
fluids in the upper limb of patients with stroke, leading training and physical factor therapy (PFT) with various physical
to stasis edema in the affected limb and shoulder-hand factors (sound, light, cold, heat, point, magnetic, and water)
pump dysfunction. This may be an essential reason for as the primary means. Although exercise therapy is an
the pathogenesis of SHS (5). Various microtraumas, such as indispensable intervention to SHS treatment, some patients
repeated blood draws, intravenous injections, or inappropriate still refuse to use the affected limb because of severe pain
active and passive motion, might also contribute to or or experience huge emotional stress. It makes it difficult for
exacerbate SHS (6, 7). them to stick to the treatment and thus reduces its expected
The current clinical treatment of post-stroke SHS focuses efficacy (15, 16). PFT (as a safe and effective alternative therapy)
on reducing pain while maintaining and restoring function not only provides anti-inflammatory, analgesic, neuromuscular
for patients. Drug treatment mainly includes oral anti- excitation, and spasticity relief via the mediating impact of
inflammatory, analgesic, immune modulating (such as electrotherapeutic stimulation but is also easily accepted by
glucocorticoids and non-steroidal anti-inflammatory drugs) patients due to the comfort of the treatment procedure (17).
and anticonvulsant and antidepressant drugs or injection of Various PFT techniques are often combined with rehabilitation
training (RT) in clinical practice to treat SHS, and its efficacy
Abbreviations: SHS, shoulder-hand syndrome; RSD, reflex sympathetic is good. However, the advantages of different PFT vary, and
dystrophy; RCTs, randomized controlled trials; NMA, network meta- there are no relevant guidelines to rank their efficacy on
analysis; PFT, physical factor treatment; FMA-UE, Fugl-Meyer upper patients with SHS, which confuses the clinical guiding practice.
extremity motor function scale; VAS, visual analog score of pain; Therefore, we aim to conduct a comprehensive review of RCTs of
RT, rehabilitation training; ET, electrotherapy; LT, light therapy; UWT, different physical factor therapies combined with rehabilitation
ultrasonic wave therapy; CHT, conductive heat therapy; PT, pressure training for the treatment of post-stroke SHS using Bayesian
therapy; MT, magnetic therapy; BFT, biofeedback therapy; EMG-BF, network meta-analysis (NMA), expecting to find the optimal
electromyographic biofeedback. physiotherapy regimen to guide clinical practice.

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Materials and methods Intervention: Acceptable treatment is mainly various


physical factor therapy (PFT) combined with rehabilitation
This study was conducted in accordance with the training (RT). PFT includes electrotherapy (ET), light therapy
Preferred Reporting Items for Systematic Reviews and (LT), ultrasound therapy (UWT), conductive heat therapy
Meta-Analyses (PRISMA) extended statement (18). This NMA (CHT), and pressure therapy (PT). As well as magnetotherapy
has been registered on the International prospective register (MT), which is based on transcranial magnetic stimulation, and
systematic reviews (PROSPERO) with the registration number biofeedback therapy (BFT), which is based on electromyography
CRD42022348743. No ethical approval or patient consent was biofeedback (EMGBF) as the main intervention. However, there
required for this study since all analyses were conducted based are no restrictions on the frequency, duration, and waveform of
on previously published studies. the above PFT.
Among them, ET contains low-frequency pulsed
electrical stimulation, transcutaneous neuromuscular electrical
Search strategy stimulation, medium-frequency electrotherapy, and ultrashort
wave; LT, infrared radiation and laser therapy; UWT, ultrasound
We conducted a comprehensive search of the following and extracorporeal shock wave; CHT, Chinese herbal wet and
databases: Web of Science, PubMed, EMBASE, Cochrane hot compresses and wax therapy; PT, air pressure, air wave
Central Controlled Trials, China Knowledge Network (CNKI), pressure therapy, and hyperbaric oxygen.
Wanfang database, VIP database, and China Biomedical Comparison: RT alone or intercomparison
Literature Database (CBM). With no restrictions on language or between interventions.
publication time, we identified the randomized controlled trials Outcomes: Primary outcomes: Fugl-Meyer Upper
(RCTs) on the observation of the efficacy of physiotherapy on Extremity Motor Function Scale (FMA-UE). Secondary
post-stroke SHS published before 1 July 2022. outcomes: Visual analog score of pain (VAS).
By combining medical subject headings (MeSH) with Study design: Randomized controlled trials only. Non-
free words using Boolean logic operators, we integrated randomized controlled studies, such as animal trials, reviews,
the following terms for a comprehensive search: “stroke,” systematic reviews, case-control studies, and study protocols,
“cerebral infarction,” “cerebral hemorrhage,” “shoulder-hand were excluded.
syndrome,” “reflex sympathetic dystrophy,” “complex localized Based on the criteria set above, two authors (GH and
pain syndrome type I,” “electrotherapy,” “low-frequency pulsed JMW) independently screened the titles and abstracts to exclude
electrical stimulation,” “neuromuscular electrical stimulation,” duplicates and studies that did not meet the inclusion criteria.
“transcutaneous electrical nerve stimulation,” “ultrasound,” Subsequently, the eligible studies were reviewed in full. Any
“ultrashort wave,” “infrared therapy,” “laser therapy,” “wax inconsistencies that arose during this period were decided
therapy,” “wet-hot compress,” “air wave pneumatic therapy,” by consensus.
“hyperbaric oxygen,” “magnetotherapy,” “transcranial magnetic
stimulation,” “biofeedback therapy,” “electromyographic
biofeedback therapy,” “rehabilitation training,” and “randomized
controlled trial.” Moreover, we manually screened the reference Data extraction and quality assessment
lists in the relevant meta-analyses and reviews to minimize the
omission of literature that meets the inclusion criteria. Taking Following the Cochrane Consumer and Communications
the PubMed search as an example, details of the search strategy Review Group’s data extraction template, we completed relevant
are shown in Supplementary Table 1. Two independent authors data collection for eligible studies: including basic publication
(SSF and MZT) processed the screening records using Endnote information (first author’s name and year of publication),
20 literature management software (Thompson ISI Research participant characteristics (total sample size, age, and duration
Soft, Philadelphia, Pennsylvania, USA). Disagreements in this of disease), interventions, duration of treatment, and quality of
process were resolved by discussion or by a third author (LHG). RCTs, among other relevant information.
The quality of each eligible study was assessed by two
independent investigators (MZT and GH) using the Cochrane
Selection and exclusion criteria Risk of Bias Tool (21). A total of seven areas were covered
(random sequence generation, allocation concealment, blinding
The inclusion of studies meeting the criteria should be based of participants and personnel, blinding of outcome assessments,
on the PICOS framework: incomplete data on outcome data, selective reporting, and other
Population: Patients were diagnosed with post-stroke SHS biases). Each item was rated as unknown, low, or high risk
according to clear diagnostic criteria (19, 20), without restriction of bias. The assessment was performed in Review Manager
to gender or age. (version 5.4).

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FIGURE 1
Literature screening process.

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Statistical analyses Results


According to the minimally informative prior distributions Search process and baseline
of the Bayesian random effects model (22), we first performed characteristics
a conventional pair-wise meta-analysis by synthesizing the
essential data from all the included studies. Evaluated effect We initially retrieved 735 literature studies, of which 343
sizes for each pair-wise treatment comparison in terms of were duplicates. After the screening of titles and abstracts,
continuous outcome, mean difference (MD) was calculated 286 documents were excluded. We reviewed the remaining
along with 95% credible intervals (CrIs) as the pooled 106 studies for full text; 6 studies were presented as case
relative effect and estimate uncertainly, respectively. As a reports or study protocols; 2 studies were diagnosed with other
visual representation of statistical heterogeneity, I 2 statistic types of disease; 11 studies did not adopt the method of
was tested to assess whether substantial heterogeneity existed. random grouping; 19 studies did not meet the inclusion criteria
The values 25, 50, and 75% indicated mild, moderate, and for this study; 13 studies did not provide relevant outcome
high heterogeneity, respectively (18). To detect whether any indicators for our analysis; 8 studies were not available in
bias was generated, a comparison-adjusted funnel plot was full text or had incomplete outcome indicators, and another 2
made as a concise description, and both were analyzed using were duplicate published studies. Thus, 45 clinical randomized
the Egger test (23). We constructed a network plot for controlled trials that meet the inclusion criteria were finally
offering all the existing relationships, with distinct treatments included (33–78).
expressed by different nodes and trials by lines joining Figure 1 depicts the processing of the literature screening.
appropriate nodes. Table 1 summarizes key characteristics such as participant
Network transitivity is the most crucial assumption baseline information and interventions in detail. The included
underlying NMA, whose assessment would affect our further studies were from China, and the literature was published
analysis directly (24). Therefore, to ensure the sufficient between 2008 and 2022. A total of 3,379 study participants were
similarity of various treatment comparisons, which can provide randomly assigned to either the trial or control group. Of these,
valid indirect inferences, we evaluate the transitivity assumption 1,696 participants were included in the trial group of seven
by comparing the clinical and methodological characteristics, different physical factor therapies combined with rehabilitation
such as the characteristics of participants and experimental training (BFT + RT, n = 135; CHT + RT, n = 352; PT + RT, n
design, across all the included studies (25, 26). In order = 259; ET + RT, n = 379; MT + RT, n = 132; UWT + RT, n =
to simulate an accurate estimation of the statistical model, 174; LT + RT, n = 265). The remaining 1,683 individuals were
four parallel Markov chains were first established in the randomized into four control groups (CHT + RT, n = 69; ET +
random selection state (27). Each chain generated 50,000 RT, n = 60; LT + RT, n = 81; RT, n = 1,473).
iterations. Due to the burn-in period, an initial 20,000
iterations were discarded to minimize the bias of initial
values when the chain reached its target distribution (28). Quality of included studies
The Brooks-Gelman-Rubin diagnostic was used to evaluate
the convergence of the models by visually inspecting the Summary tables of individual and overall level quality
historical trajectory of trace combined with density plots (29) assessments are detailed in Supplementary Figures 2, 3. All 45
(see Supplementary Figure 1 for details). As the estimated studies (33–78) reported group randomization, but allocation
probability of ranking the physical treatments, the surface concealment was unclear. Due to intervention limitations, only
under the cumulative ranking curve (SUCRA) was presented two studies (33, 40) adopted the single-blind method for
as a simple numerical summary statistic cumulative ranking participants; four studies (40, 59, 71, 75) evaluated the study
probability plot for each treatment (30). SUCRA with a higher results using the blind method. Five studies (36, 41, 45, 63,
value denotes a greater likelihood of a given treatment being in 65) reported detailed cause shedding. All 45 included studies
the top rank or highly effective. In contrast, the value “zero” reported on the pre-specified outcomes completely. In addition,
indicates that the treatment is sure to be the worst. Finally, two studies (44, 60) mentioned no adverse effects.
to explore whether potential source inconsistency arises in our
network, we use the “node splitting” technique, comparing
direct and indirect evidence across the network (when P > Network analysis results
0.05 indicates that consistency arises) (31, 32). The above
analyses were performed using the “Gemtc” package (version Primary outcome: FMA-UE
1.0–1) and “rjags” (version 4–13) in R software (version The preliminary conventional meta-analysis observed a high
4.1.3), and STATA (version 16.0) software (StataCorp, College degree of heterogeneity in the FMA-UE score among studies
Station, TX, USA). (I2 = 88.2%, P = 0.000). The adjusted funnel plots showed

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TABLE 1 Characteristics of included studies.

Study ID Participant Age Gender (M/F) Interventions Course Outcome


T C T C
Zhang et al. (79) 100 100 T: 57.10 ± 1 0.88 T: 57/43 CHT + RT RT 30d FMA-UE

C: 56.30 ± 10.72 C: 59/41 VAS

Zhao et al. (80) 51 50 T: 58.12 ± 2.41 T: 27/24 LT + RT RT 28d FMA-UE

C: 57.89 ± 2.37 C: 27/23

Tian et al. (81) 28 29 T: 65.90 ± 9.50 T: 15/13 MT + RT RT 2w FMA-UE

C: 66.97 ± 10.51 C: 14/15 VAS

Wu (33) 28 28 T: 59.4 ± 10.7 T: 15/13 MT + RT RT 27d FMA-UE

C: 58.5 ± 9.5 C: 15/13 VAS

Li et al. (34) 25 25 T: 62.28 ± 13.79 T: 22/3 UWT + RT RT 4w FMA-UE

C: 61.68 ± 11.91 C: 20/5 VAS

Liu and Wang (35) (a) 50 50 T: 60.2 ± 10.8 T: 29/21 MT + RT RT 2w FMA-UE

C: 62.7 ± 10.7 C: 27/23 VAS

Ren et al. (40) 40 40 T: 51.64 ± 7.47 T: 22/18 CHT + RT RT 4w FMA-UE

C: 57.28 ± 10.66 C: 24/16 VAS

Chen and Zheng (43) 27 27 T/C: 63.8 ± 8.4 / BFT + RT CHT + RT 4w FMA-UE

VAS

Li and Lai (42) 40 40 T: 62.2 ± 8.9 T: 23/17 ET + RT RT 4w FMA-UE

C: 61.7 ± 9.3 C: 24/16 VAS

Zhang et al. (41) (a) 30 30 T: 60.1 ± 7.31 T: 18/12 ET + RT RT 4w FMA-UE

C: 59.1 ± 7.9 C: 19/11 VAS

Weng et al. (46) 30 30 T: 68.82 ± 3.34 T: 18/12 CHT + RT RT 4w FMA-UE

C: 68.85 ± 3.36 C: 19/ 11 VAS

Li (50) 15 15 T: 48.7 ± 5.3 T: 10/5 PT + RT RT 21d VAS

C: 46.5 ± 6.8 C: 8/7

Wu et al. (51) 30 30 T: 54.5 ± 6.5 T: 18/12 PT + RT RT 18d FMA-UE

C: 56.2 ± 7.6 C: 16/14

Cai et al. (55) 37 33 T: 57.14 ± 3.99 T: 17/20 ET + RT RT 47d FMA-UE

C: 58.36 ± 4.48 C: 16/17 VAS

Lin et al. (56) 42 42 T: 63.1 ± 8.3 T: 24/18 BFT + RT CHT + RT 4w FMA-UE

C: 62.5 ± 9.2 C: 25/17 VAS

Li et al. (57) (a) 30 30 T: 64.7 ± 16.9 T: 19/11 UWT + RT ET + RT 4w FMA-UE

C: 65.4 ± 17.3 C: 17/13 VAS

Hu et al. (65) 36 36 T: 61.2 ± 17.8 T: 20/16 PT + RT RT 4w FMA-UE

C: 60.1 ± 18.2 C: 21/15 VAS

She et al. (64) 30 30 T: 57.39 ± 3.18 T: 18/12 ET + RT RT 4w FMA-UE

C: 59.13 ± 4.53 C: 16/14 VAS

Zhao and Ma (66) 25 25 T: 63.3 ± 4.6 T: 18/7 LT + RT RT 20d FMA-UE

C: 60.2 ± 5.8 C: 16/9

(Continued)

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TABLE 1 (Continued)

Study ID Participant Age Gender (M/F) Interventions Course Outcome


T C T C
Zhang et al. (67) 35 33 T: 61.4 ± 10.9 T: 20/15 ET + RT RT 3w VAS

C: 60.8 ± 11.3 C: 20/13

Liu and Dong (71) 20 20 T: 63.7 ± 11.4 T: 14/6 ET + RT RT 3w FMA-UE

C: 62.8 ± 12.1 C: 13/7 VAS

Su and Chen (72) 30 30 T: 61 T: 19/11 PT + RT RT 30d FMA-UE

C: 63 C: 18/12 VAS

Yang et al. (36) 31 31 T: 71.81 ± 9.95 / ET + RT RT 4w VAS

C: 72.42 ± 9.68

Liu et al. (37) (b) 40 39 T: 63.38 ± 9.22 / ET + RT RT 2w FMA-UE

C: 64.21 ± 9.35 VAS

Qiao and Ding (39) 51 51 T: 53.45 ± 5.48 T: 22/29 CHT + RT LT + RT 28d FMA-UE

C: 53.56 ± 5.34 C: 23/28 VAS

Gong et al. (45) 30 30 / / CHT + RT LT + RT 21d FMA-UE

VAS

Guo and Ruan (62) 60 60 T: 63.1 ± 3.2 T: 36/24 CHT + RT RT 3w VAS

C: 61.1 ± 2.6 C: 37/23

Zhou et al. (49) 20 20 T: 63.71 ± 6.45 T: 16/4 ET + RT RT 6w FMA-UE

C: 63.12 ± 6.89 C: 15/5 VAS

Yuan and Chen (59) 40 40 T: 51.73 ± 11.16 T: 24/16 PT + RT RT 10d FMA-UE

C: 51.66 ± 11.01 C: 22/18 VAS

Shi et al. (61) 40 40 T: 52.73 ± 11.17 T: 24/16 ET + RT RT 4w FMA-UE

C: 52.65 ± 10.03 C: 22/18 VAS

Guo and Ruan (62) 36 31 T: 52 T: 25/12 BFT + RT RT 4w FMA-UE

C: 48 C: 19/12 VAS

Wang et al. (63) 40 40 T: 65.8 ± 12.6 T: 27/13 LT + RT RT 4w FMA-UE

C: 66.3 ± 12.6 C: 23/17 VAS

Liu et al. (68) 46 46 T: 62.4 ± 9.6 T: 29/17 PT + RT RT 4w FMA-UE

C: 61.4 ± 10.2 C: 28/19 VAS

Zhang and Huang (70) 45 45 T: 52.63 ± 9.67 T: 25/20 PT + RT RT 15d FMA-UE

C: 51.26 ± 10.13 C: 26/19 VAS

Yang et al. (50) 56 56 T: 56.85 ± 10.7 T: 31/25 ET + RT RT 14d FMA-UE

C: 56.72 ± 10.12 C: 29/27

Tan (48) 41 41 T: 56.56 ± 3.34 T: 23/18 CHT + RT RT 10d FMA-UE

C: 56.23 ± 3.16 C: 24/17 VAS

Bao et al. (38) 30 30 T: 63.32 ± 6.13 T: 16/14 UWT + RT RT 4w FMA-UE

C: 64.82 ± 8.27 C: 16/14 VAS

Zhang et al. (44) (b) 29 29 T: 53.91 ± 5.33 T: 13/16 UWT + RT RT 4w FMA-UE

C: 53.70 ± 5.73 C: 15/14 VAS

(Continued)

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TABLE 1 (Continued)

Study ID Participant Age Gender (M/F) Interventions Course Outcome


T C T C
Zhang and Huang (47) 26 26 T: 51.31 ± 7.32 T: 16/10 MT + RT RT 4w FMA-UE

C: 53.18 ± 9.40 C: 17/9 VAS

Liu et al. (74) 32 31 T: 58.84 ± 6.12 T: 17/15 PT + RT RT 30d FMA-UE

C: 60.04 ± 5.95 C: 18/13 VAS

Wang et al. (60) 54 54 T/C: 55.27 ± 13.5 / LT + RT RT 4w FMA-UE

Xue et al. (54) 30 30 T: 62.7 ± 5.4 T: 15/15 BFT + RT RT 6w FMA-UE

C: 63.4 ± 6.7 C: 14/16

Yan et al. (82) 30 30 T: 53.52 ± 15.32 T: 16/14 UWT + RT RT 4w FMA-UE

C: 53.85 ± 15.13 C: 17/13

Lu et al. (58) 80 80 T: 62.2 ± 4.9 T: 46/34 LT + RT RT 4w FMA-UE

C: 63.4 ± 4.9 C: 44/36 VAS

Li et al. (57) (b) 30 30 T: 64.7 ± 16.9 T: 19/11 UWT + RT ET + RT 2w FMA-UE

C: 65.4 ± 17.3 C: 17/13 VAS


ET, electrotherapy; LT, light therapy; UWT, ultrasonic wave therapy; CHT, conduction heat therapy; PT, pressure therapy; MT, magnetic therapy; BFT, biofeedback therapy; RT,
rehabilitation training; FMA-UE, fugl-meyer upper extremity motor function scale; VAS, visual analog score of pain; C, control group; T, treatment group; d, day; w, week.

a relatively symmetrical distribution of studies on both sides [MD = 5.91 95%CrI (2.07, 9.76)]; CHT + RT [MD = 4.06
of the inverted funnel. However, some smaller studies are 95%CrI (1.19, 6.93)]; and PT + RT [MD = 3.30 95%CrI
distributed below and outside the inverted funnel, suggesting the (0.13, 6.48)] were all superior to LT + RT. Meanwhile, BFT
possible presence of publication bias (Supplementary Figure 1). + RT [MD = 4.23 95%CrI (0.37, 8.09)] also outperformed ET
An additional Egger’s test was used for secondary verification + RT.
of the presence of publication bias, which showed P = 0.933 We plotted SUCRA lines to rank each intervention
(>0.05), indicating that there is no publication bias in this study category (Figure 3 and Supplementary Figure 5) and compared
(Supplementary Table 2). them with other interventions. BFT+RT (SUCRA = 94.7%)
We constructed a visual network geometry showing all the had the highest probability of improving upper extremity
main evidence of the interventions. Each node represents one motor function in patients with post-stroke SHS, followed
intervention, and its size depends on the number of patients by two equally remarkable interventions CHT+RT (SUCRA
directly studied. As shown in Figure 2, the most common = 76.0%) and PT+RT (SUCRA = 65.6%), and the fourth-
intervention method was ET + RT with nine groups studied (n ranked UWT+RT (SUCRA = 62.3%). In contrast, MT+RT
= 313), followed by PT + RT (n = 259) involving seven groups, (SUCRA = 42.3%), ET+RT (SUCRA = 39.3%), and LT+RT
CHT + RT (n = 292) and UWT + RT (n = 174) involving six (SUCRA = 19.8%) had relatively low probabilities, while
groups, and LT + RT (n = 265) involving five groups. Two other the probability of RT (SUCRA = 0%) was the lowest.
interventions [BFT + MT (n = 135) and MT + RT (n = 132)] The existence of inconsistencies between direct and indirect
involved four groups. evidence was assessed by the “nodal split” method. The results
In terms of the outcome of FMA-UE, the efficacy of various (Supplementary Figure 6) showed that there are no significant
physical factor therapies (PFT) combined with rehabilitation inconsistencies in each branch of the entire network (P > 0.05)
training (RT) post-intervention is shown in Figure 3. BFT + [CHT + RT vs. RT (P = 0.566); LT + RT vs. RT (P = 0.123);
RT [MD = 10.21 95%CrI (6.85, 13.58)]; CHT + RT [MD = UWT + RT vs. RT (P = 0.496); ET + RT vs. RT (P = 0.498);
8.36 95%CrI (5.91, 10.82)]; PT + RT [MD = 7.60 95%CrI BFT + RT vs. RT (P = 0.321); LT + RT vs. CHT + RT (P
(5.41, 9.80)]; UWT + RT [MD = 7.41 95%CrI (4.86, 9.96)]; = 0.123); BFT + RT vs. CHT + RT (P = 0.325); and ET +
MT + RT [MD = 6.06 95%CrI (3.09, 9.02)]; ET + RT [MD RT vs. UWT + RT (P = 0.50)]. Thus, we obtained a valid
= 5.98 95%CrI (4.09, 7.88)]; and LT + RT [MD = 4.30 comparison of the above-mentioned different physical therapy
95%CrI (2.00, 6.60)] efficacy were all statistically significant interventions to improve the function of the upper limb of SHS
and significantly superior to the control group. BFT + RT after stroke.

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FIGURE 2
The network evidence graph for FMA-UE. RT, rehabilitation training; ET, electrotherapy; LT, light therapy; UWT, ultrasonic wave therapy; CHT,
conduction heat therapy; PT, pressure therapy; MT, magnetic therapy; BFT, biofeedback therapy.

Secondary outcome: VAS [MD = −1.92 95%CrI (−2.53, −1.31)]; CHT + RT [MD =
The I2 values indicated that our preliminary meta- −1.57 95%CrI (−2.12, −1.03)]; ET + RT [MD = −1.33 95%CrI
analysis showed high heterogeneity in VAS scores across all (−1.80, −0.85)]; UWT + RT [MD = −1.28 95%CrI (−1.99,
included studies (I2 = 82.2%, P = 0.000). Comparison-adjusted −0.57)]; and MT + RT [MD = −1.94 95%CrI (−1.94, −0.40)].
funnel plot suggested that the occurrence of publication bias In addition, BFT + RT [MD = −1.49 95%CrI (−2.59, −0.40)];
depends on several scattered points that are asymmetrically PT + RT [MD = −1.31 95%CrI (−2.29, −0.33)]; and CHT +
distributed below and outside the inverted funnel plot RT [MD = −0.96 95%CrI (−1.73, −0.20)] were also significantly
(Supplementary Figure 7). In addition, Egger’s test confirmed superior than LT + RT.
this result (P = 0.011) (Supplementary Table 3). Plotting the SUCRA line to rank each intervention’s
The network diagram is shown in Figure 4, including seven efficacy in pain relief (Figure 5 and Supplementary Figure 8)
interventions and four control groups. ET + RT was the most showed that BFT + RT (SUCRA = 89.9%) obtained the
frequent intervention and investigated in 9 arms (n = 303), best probability compared to the other seven interventions.
followed by the most common intervention of CHT + RT (n However, PT + RT (SUCRA = 84.9%) and CHT + RT
= 352) and PT + RT (n = 244) involving 7 arms; UWT + RT (n (SUCRA = 65.8%) also got a remarkable ranking among
= 144) involving 5 arms; MT + RT (n = 132) involving 4 arms; them, followed by ET + RT (SUCRA = 50.1%); UWT
BFT + RT (n = 105) involving 3 arms; and LT + RT (n = 120) + RT (SUCRA = 48.3%); and MT + RT (SUCRA =
was the least involving only 2 arms. 41.9%). LT + RT (SUCRA = 18.3%) and RT (SUCRA =
The clinical efficacy of VAS pain relief results showed 0.9%) ranked last. The node-splitting model results showed
(Figure 5) that when compared with the control group, except (Supplementary Figure 9) no significant inconsistency between
for LT + RT, the other interventions showed better efficacy: the direct and indirect evidence (P > 0.05), so the current
BFT + RT [MD = −2.10 95%CrI (−3.01, −1.20)]; PT + RT evidence is reliable.

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FIGURE 3
Relative effect sizes of FMA-UE efficacy after the intervention according to network meta-analysis. Treatments were ranked in order of their
likelihood of being the best treatment. The numbers in the blue boxes are SUCRA values, representing the rank of the treatments. Meaningful
pairwise comparisons are highlighted in green and bold. RT, rehabilitation training; ET, electrotherapy; LT, light therapy; UWT, ultrasonic wave
therapy; CHT, conduction heat therapy; PT, pressure therapy; MT, magnetic therapy; BFT, biofeedback therapy.

Discussion resistance psychology in some patients, affecting their treatment


outcomes (20, 83). Evidence suggests that combining two
Existing RCTs have only analyzed the relative effectiveness or more therapies may be more effective than rehabilitation
of individual physical therapy interventions in terms of their alone in improving the post-stroke SHS symptoms of patients.
respective efficacy in patients with post-stroke SHS. At the Physical therapy, in particular, has shown superior performance
same time, traditional meta-analyses have only been used in reducing pain and improving motor function as the first-
to assess the effectiveness of a particular intervention. It all line treatment choice for this disease (17, 84–86). Among
lacks comprehensive comparative analyses between studies, but them, biofeedback therapy (BFT) with EMG biofeedback as
the NMA overcomes this limitation. Network meta-analysis the primary intervention combined with rehabilitation training
integrates at least two or more physical interventions by (RT) may offer the potential for the treatment of SHS. In this
performing direct and indirect cross-comparisons with the study, both FMA and VAS results showed that BFT + RT [(MD
help of techniques that adjust indirect comparisons while = 10.21 95%CrI (6.85, 13.58), (SUCRA = 94.7%); (MD = −2.10
assessing their effectiveness and performing relative ranking on 95%CrI (−3.01, −1.20), (SUCRA = 89.9%)] is the best treatment
all physical therapy interventions included (75). To the best of strategy to improve upper limb motor function and reduce pain
our knowledge, this is the first study to use the NMA approach in patients with SHS.
to compare the efficacy of different physical therapy for patients Electromyographic biofeedback (EMG-BF) therapy, a
with SHS after stroke. This complex integrated approach is branch of biofeedback therapy (BFT), combines biofeedback
superior to most previous studies, and it can be used as an techniques with electrical stimulation to promote the
evidence-based clinical guideline to provide reference evidence reconstruction of undamaged nerve cells and the development
for the selection of optimal protocols for the future clinical of new neural networks after stroke (84). By amplifying the
treatment of SHS. bioelectrical activity of muscle tissue, which the patient is
Post-stroke SHS is a complex disease that threatens the unaware of under normal circumstances, and processing the
recovery of patients with stroke, and it is essential to identify signal, the signal is fed back to the human body as intuitive
effective treatment strategies. Although rehabilitation is effective visual and auditory signals and further fed back to the brain
in treating SHS, pain is the primary reason that prevents center. The brain control center regulates muscle contraction
patients from receiving SHS treatment. In addition, it leads to and diastole intensity based on the feedback signal and receives

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FIGURE 4
The network evidence graph for VAS. RT, rehabilitation training; ET, electrotherapy; LT, light therapy; UWT, ultrasonic wave therapy; CHT,
conduction heat therapy; PT, pressure therapy; MT, magnetic therapy; BFT, biofeedback therapy.

active rehabilitation training to achieve the goal of training and patients with SHS can improve patients’ ability to control
treatment (85). According to the results of the meta-analysis and regulate random movements significantly. Meanwhile,
of this study, we found that there are statistical differences it also stimulates their desire to train, which transforms
in the comparison of the efficacy of BFT + RT and electrical passive rehabilitation into active rehabilitation, and improves
stimulation therapy (ET) combined with RT [MD = 4.23 patients’ compliance with training, leading to improved
95%CrI (0.37, 8.09)] in improving limb motor function. The patient outcomes.
results also confirmed the advantages of EMGBF treatment. It In contrast, the potential mechanism of EMG biofeedback
overturns the traditional notion that autonomic nerves cannot in pain relief remains unclear. Related studies found (90) that
be controlled arbitrarily and allows patients to dynamically through the “stimulation-feedback” mode, EMGBF is capable
access electromyographic physiological information at the of converting subtle EMG signals into visual stimuli, thereby
site of information collection, enabling them to learn to motivating patients to engage in active exercises of the core
consciously regulate their psychophysiological activity to muscles of the affected shoulder to stabilize the shoulder
treat somatic disorders (86). It has been demonstrated (87) joint and alleviate pain. The problem is that when hemiplegic
that EMG-BF provides an additional benefit for the recovery shoulder pain is caused by the interaction of multiple etiologies,
of limb function in patients with stroke when combined a single therapy may not be able to achieve the desired
with conventional rehabilitation. Moreover, its efficacy is level of pain relief (91, 92). However, our study draws the
undoubtedly substantial. In addition to promoting the recovery opposite conclusion, which may be related to our combing EMG
of neurological deficits after stroke, it also helps patients biofeedback with rehabilitation training and thus improved
overcome pain-induced resistance to training and motivates efficacy; or it may be associated with the lack of direct evidence
them to participate actively in rehabilitation (88, 89). Related between interventions. Speculation on this contradictory view
studies (43) found that using surface EMG-BF to treat stroke still needs to be validated by more extensive RCTs of the

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FIGURE 5
Relative effect sizes of VAS efficacy after the intervention according to network meta-analysis. Treatments were ranked in order of their
likelihood of being the best treatment. The numbers in the blue boxes are SUCRA values, representing the rank of the treatments. Meaningful
pairwise comparisons are highlighted in green and bold. RT, rehabilitation training; ET, electrotherapy; LT, light therapy; UWT, ultrasonic wave
therapy; CHT, conduction heat therapy; PT, pressure therapy; MT, magnetic therapy; BFT, biofeedback therapy.

combined treatment with myoelectric biofeedback on shoulder alleviate pain, and relax tendons have many advantages. It can
pain in the future. dilate the local blood vessels and open pores, which deepens the
Also noteworthy is that CHT + RT and PT + RT drug penetration and gives full play to its effect. Consequently, it
rank relatively high among all interventions and can be improves the time effect of pain symptom relief and facilitated
used adjunctively for post-stroke SHS. CHT mainly consists the metabolism of inflammation and edema. Additionally,
of paraffin wax therapy and moist heat compress therapy. it significantly increased blood flow to the affected limb’s
Wax therapy, as a particular conductive medium, uses this tissues, lowered muscle and ligament tension, and enhanced
principle of warming to conduct heat through the skin to the flexibility of joints and limb movements, thus improving
deep tissues, accelerating tissue repair, promoting cellular therapeutic results (95, 96). They have limitations, however,
metabolism, reducing the tension of tissue fibers, and increasing and should be used with caution in patients who have the
their elasticity. It thereby facilitates muscle strength recovery bleeding tendency in clinical, local sensory abnormality, or wax
and enhances joint mobility. At the same time, the warming allergy (86).
effect can reduce the excitability of the nerve, improve blood Pressure therapy (PT) mainly refers to interstitial pneumatic
circulation, and finally, reduce inflammatory edema, and therapy. With the use of an air pump, the multi-chambered
accelerate the removal of pain-causing mediators. Furthermore, balloon is inflated uniformly and decompressed in an orderly
when the wax is cooled, its fixed condition exerts a local manner, providing centripetal compression from distal to
oppressive impact on the body’s tissues, aiding in the eradication proximal segments of the limb and improving arterial perfusion.
of swelling and having a better effect on the relaxation of the It effectively improves arterial blood circulation in the affected
affected joint ligaments, muscles, and tendons (93). Clinical limb, thereby eliminating edema and improving peripheral
studies have demonstrated that functional training of the vascular function (66, 97). However, given that pneumatic
upper extremity soon following the wax therapy can help therapy inflation and deflation are neither based on blood
patients better participate in the training and complete their flow blockage and recovery pressure nor does it take into
rehabilitation activities better (46, 94). Wet heat compress account the influence of the patient’s upper limb circumference
therapy, also referred to as Chinese herbal medicine moist on the pneumatic therapy pressure, and that patients with
heat compress therapy, is often combined with Chinese herbal stroke frequently have sensory impairment of the affected limb,
medicine. Using the combined effects of herbal efficacy and judging the pneumatic therapy pressure based on the patient’s
physical thermal effect to select herbs that reduce inflammation, subjective sensation alone lacks scientific validity and may cause

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Feng et al. 10.3389/fneur.2022.1056156

adverse effects (98). Consequently, pneumatic therapy has been such as transcutaneous electrical nerve stimulation,
used in relatively few RCTs to treat this disease alone, mainly intermediate frequency electrotherapy, and hyperbaric
as adjunctive therapy after rehabilitation training to provide oxygen or confounding factors such as different frequencies and
muscle relaxation and pain relief. As previously stated, our different intervention durations. Second, the included studies
findings also found that PT + RT is more effective in relieving which were all from China lack ethnic diversity, which may
pain (SUCRA = 84.9%) than improving limb motor function result in the limited generalizability of the findings. Finally,
(SUCRA = 65.6%). significant differences in sample sizes between physical therapy
In addition, studies showed (99, 100) that ultrasonic wave interventions may also have contributed to imprecise analyses.
therapy (UWT) also has mechanical and thermal physical Compared with the overall sample size (n = 3379), the sample
effects. By directly acting on local subcutaneous tissue, the sizes of BFT + RT (n = 135) and MT + RT (n = 132) are
ultrasound emitted from outside the body is concentrated in relatively small.
the deep surface of the tissue and produces a high-energy
point, which causes the lesion tissue to absorb energy in
a short period of time and rapidly heat up, and produces
Conclusion
physical and chemical effects. Ultimately, it promotes local
Based on the findings of our NMA study, EMG biofeedback
blood circulation, accelerates the absorption of inflammatory
therapy combined with rehabilitation training (BFT + RT) is
factors, reduces the excitability of sensory nerves, and cures pain.
the most effective physiotherapy option for improving upper
However, based on the evidence of this study, UWT did not
extremity motor function and relieving pain in patients with the
present a prominent advantage, especially in terms of pain relief
post-stroke SHS, followed by CHT + RT and PT + RT. However,
(SUCRA = 48.3%). This may be related to the lack of significant
given the macroscopic nature of this study and the lack of direct
differences between various physical therapy interventions and
comparative evidence between multiple countries and centers,
may also be influenced by the number of relevant RCTs available
future studies need to conduct related randomized controlled
for inclusion, resulting in a lack of more direct comparative
trials on more physiotherapy interventions. In addition, it helps
evidence. Similarly, the relatively weak ranking of magnetic
to conduct more relevant and refined meta-analyses successfully.
therapy (MT) with transcranial magnetic stimulation as the
main intervention may be explained by the relative paucity
of studies on the clinical use of magnetic therapy for SHS Data availability statement
compared to others (n = 132). Nevertheless, again, this needs
further confirmation. The original contributions presented in the study are
More noteworthy is that, according to our pooled meta- included in the article/Supplementary material, further inquiries
analysis, no statistical difference was observed in pain relief can be directed to the corresponding author.
between the light therapy combined with rehabilitation training
(LT + RT) group and the control group. Also, based on the
SUCRA values, the top three ranked physiotherapies (BFT Author contributions
+ RT, CHT + RT, PT + RT) are all statistical differences
compared to LT + RT. Generally, this finding is consistent with SF conceived the study and wrote the manuscript. MT, GH,
recent studies (101), indicating that phototherapy has a weak and JW participated in the extraction and analysis of the data.
immediate analgesic effect and that its long-term effectiveness The study was critically supervised, evaluated, and validated by
is mainly determined by its ability to repair tissues. Therefore, it LG, SH, and DL. All of the authors worked on the article and
is commonly used in the adjunctive treatment of pain diseases. agreed with the version that was sent in.
On the contrary, the possible differences in the methodological
design of different current studies result from the continuous
Funding
advancement of medicine and the emergence of new high-
energy lasers and helium-neon lasers. However, due to the
This study was supported by the National Natural Science
setting of inclusion criteria and other technical limitations, we
Foundation of China (grant number. 81860878) and the Yunnan
failed to explore this aspect in depth. This remains to be analyzed
Provincial Education Department Scientific Research Fund
in the future by further collecting more direct evidence.
Project (grant number. 2022Y375).

Limitations Acknowledgments
However, our study has some limitations as well. First, The author would like to thank her friends Yiqin Zhong
our study aims to make comparisons from a macroscopic and Ting Zeng for their help in editing and revising this
perspective, thus ignoring the refined specific interventions manuscript’s images.

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Feng et al. 10.3389/fneur.2022.1056156

Conflict of interest SUPPLEMENTARY FIGURE 2


Quality assessment percentage graph.

The authors declare that the research was conducted in the SUPPLEMENTARY FIGURE 3

absence of any commercial or financial relationships that could Summary chart of quality assessment.

be construed as a potential conflict of interest. SUPPLEMENTARY FIGURE 4


FMA-UE funnel plot.

Publisher’s note SUPPLEMENTARY FIGURE 5


Probability ranking results of FMA-UE of different interventions.

All claims expressed in this article are solely those of the SUPPLEMENTARY FIGURE 6
Node-splitting diagram of FMA-UE.
authors and do not necessarily represent those of their affiliated
organizations, or those of the publisher, the editors and the SUPPLEMENTARY FIGURE 7
VAS funnel plot.
reviewers. Any product that may be evaluated in this article, or
claim that may be made by its manufacturer, is not guaranteed SUPPLEMENTARY FIGURE 8

or endorsed by the publisher. Probability ranking results of VAS of different interventions.

SUPPLEMENTARY FIGURE 9
Node-splitting diagram of VAS.
Supplementary material
SUPPLEMENTARY TABLE 1
The search strategy for PubMed.
The Supplementary Material for this article can be
found online at: https://www.frontiersin.org/articles/10.3389/ SUPPLEMENTARY TABLE 2

fneur.2022.1056156/full#supplementary-material Egger’s test for FMA-UE.

SUPPLEMENTARY FIGURE 1 SUPPLEMENTARY TABLE 3


Model convergence and density plots. Egger’s test for VAS.

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