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817709 AIM Li and Deng

acupuncture
IN MEDICINE
Original paper

Acupuncture in Medicine
Acupuncture combined with swallowing 2019, Vol. 37(2) 81­–90
https://doi.
DOI: 10.1136/acupmed-2016-011305

training for poststroke dysphagia: a


org/10.1136/acupmed-2016-011305
© The Author(s) 2019
Article reuse guidelines:
sagepub.com/journals-permissions
meta-analysis of randomised journals.sagepub.com/home/aim

controlled trials

Ling Xin Li1 and Kai Deng2

Abstract
Objective: This meta-analysis aimed to assess the efficacy and safety of the combination of acupuncture with swallowing
training for poststroke dysphagia.
Method: Nine electronic databases (including PubMed and China National Knowledge Infrastructure) were searched
from their inception through June 2016. Seventeen studies were included in this meta-analysis. Data on 1479 eligible
patients were extracted, and the relative risk (RR) and standard mean difference (SMD) with 95% CI for the effective
rate (ER), swallowing function assessment (SFA), individual activity (IA), eg., modified Barthel Index (MBI) and quality of
life (QOL) were evaluated.
Results: The pooled ER (RR 1.26, 95% CI 1.19 to 1.34, P<0.001, 14 studies) and SFA (SMD 1.06, 95% CI 0.79 to 1.32,
P<0.001, five studies) suggested that combination therapy yielded a significantly higher ER and improved the SFA scores
to a greater degree than swallowing training alone in patients with poststroke dysphagia. The pooled QOL score (SMD
1.06; 95% CI −0.04 to 2.17, P=0.06, two studies) did not differ between groups. The MBI data (SMD 1.47, 95% CI 1.07 to
1.87, P<0.001, one study) showed significant improvement in IA. Some evidence of publication bias was observed for the
ER, although the trim-and-fill analysis and fail-safe number indicated no influence of publication bias on its pooled effect
size. There was no evidence of publication bias of any other outcome measures.
Conclusion: This study showed that acupuncture combined with swallowing training may improve the ER, swallowing func-
tion and activities of daily life of patients with poststroke dysphagia compared with conventional swallowing training alone.

Keywords
post-stroke dysphagia, acupuncture, swallowing training, effective rate, swallowing function assessment, individual activity,
quality of life

Accepted: 22 October 2017

Introduction difficulties in stroke patients. Many studies have suggested


that acupuncture10–16 and swallowing training9,17 may be
Dysphagia is a common complication in stroke patients, with
a reported incidence of 34.7%–44%.1 It is characterised by
swallowing difficulty in the oropharyngeal phase, especially 1Department of Rehabilitation Medicine, West China Hospital, Sichuan
for liquids,2 and can lead to aspiration pneumonia, nasogas- University, Chengdu, China
2Department of Gastroenterology, West China Hospital, Sichuan
tric tube placement and even death.3–5 Dysphagia has also
University, Chengdu, China
been associated with quality of life (QOL) issues, such as
social anxiety, withdrawal and depression.6,7 The currently LXL and KD contributed equally.
available management strategies for dysphagia, such as acu-
Corresponding author:
puncture or swallowing training, are temporary and have Dr Ling Xin Li, Department of Rehabilitation Medicine, West China
relatively limited effectiveness.8,9 Consequently, multidisci- Hospital, Sichuan University, Chengdu, Sichuan 610041, China.
plinary approaches are essential to address swallowing Email: lilingxinlsh@163.com

Acupuncture in Medicine, 37(2)


82 Acupuncture in Medicine

beneficial for dysphagia in stroke patients, but whether the and KD). Information on the following items was collected
combination of acupuncture and swallowing training leads to for each trial: first author, publication year, study period,
greater improvements in swallowing function than swallow- number of eligible cases, age, gender, duration, the acu-
ing training alone remains unclear. Thus, we aimed to per- puncture and swallowing training regimen, and data related
form a meta-analysis to investigate the effectiveness of to ER, SFA, IA, QOL and AE. Disagreements were settled
combination therapy for treating dysphagia in patients with by discussion and consensus between the two authors.
stroke versus conventional care alone.
Quality assessment
Methods The quality of the methodology of the extracted studies was
Search strategy independently assessed by the two reviewers (LXL and
KD) using the Cochrane risk of bias tool.19 Any disagree-
Comprehensive electronic and manual searches were con- ments regarding study selection or discrepancies in the rat-
ducted in nine databases (PubMed, OVID (MEDLINE, ings were resolved through discussion.
EMBASE), ISI (Science Citation Index Expanded), EBSCO
(Academic Source Premier), the Cochrane Library, China
National Knowledge Infrastructure, China Biology Medicine, Statistical analyses
Wanfang and VIP) from their inception through 16 June 2016. The effect sizes were the relative risk (RR) and 95% CI
The references cited in the searched articles were also for dichotomous data and the standard mean difference
reviewed. The search strategy was designed and performed (SMD) with 95% CI for continuous data. Statistical het-
independently by two authors (LXL and KD) and is detailed in erogeneity among the included studies was assessed
online supplemental appendix 5; if discrepancies occurred, using the I2 statistic, for which P<0.10 and I2 >50% rep-
consensus was reached through consultation. If multiple stud- resented substantial heterogeneity.20 The following pro-
ies were identified by the same research group, we included cedure was applied to explain any type of heterogeneity
the paper that had the most complete information. Searches that existed: (1) sensitivity analysis; (2) subgroup analy-
were limited to studies published in English and Chinese. sis and meta-regression; and (3) a random-effects model
using the DerSimonian-Laird method.21 Publication bias
Study selection was assessed with: (1) funnel plots and Begg’s test/
Egger’s test22; (2) a trim-and-fill adjusted analysis; and
Decisions regarding study eligibility were independently (3) the fail-safe number (Nfs).23 The statistical analysis
made by the two authors (LXL and KD). The inclusion crite- was performed using Statistics Data Analysis Special
ria were as follows: (1) patients: all of the participants had Edition software (Stata SE, V.12.0; Stata Corp LP,
been diagnosed with ischaemic or haemorrhagic stroke by College Station, Texas, USA).
CT or MRI and were clinically confirmed to have dysphagia;
(2) study design: the trials had to be randomised controlled
trials (RCTs, not including quasi-RCTs) that aimed to com- Results
pare combination therapy with swallowing training alone;
Study inclusion and characteristics
(3) outcomes: the primary outcomes were the clinical effec-
tive rate (ER), swallowing function assessment (SFA), indi- A total of 1142 relevant references were initially retrieved.
vidual activity (IA; eg, the modified Barthel index (MBI)) Ultimately, 17 studies24–40 were included in the meta-analy-
and QOL (eg, swallowing-related QOL (S-QOL)); adverse sis. The search results are shown in the flowchart in Figure
events (AEs) were considered secondary outcomes. The 1. The eligible cases totalled 1479 patients: 745 in the
exclusion criteria were as follows: (1) non-original research experimental groups and 734 in the control groups. All 17
articles; (2) studies that were not published in English or of the included RCTs were conducted in China; 16 were
Chinese; and (3) studies in which the required data were una- published in Chinese and 1 was published in English. These
vailable. Any disagreements were resolved by the two review included trials were reported from January 2004 to
authors through discussion and consultation when necessary. November 2016. Among the acupuncture regimens, the
Figure 1 shows the flowchart of the study selection proce- nine most commonly used acupuncture points were GB20
dure, which was presented in accordance with the Preferred (Fengchi), GB12 (Wangu) and TE17 (Yifeng) in the nape,
Reporting Items for Systematic Reviews and Meta-Analyses CV23 (Lianquan) and Pang Lianquan (0.8–1 cun from
2009 guideline.18 CV23) in the neck, and Jinjin, Yuye and Yanhoubi (on the
posterior pharyngeal wall) in the mouth. The swallowing
training protocol primarily consisted of functional training
Data extraction and feeding-swallowing training. The training consisted of
The retrieved studies were carefully assessed, and the data 12–90 sessions (5–45 min per session) and lasted from 2
were independently extracted by the two researchers (LXL weeks to 2 months. The outcome measurements included:

Acupuncture in Medicine, 37(2)


Li and Deng 83

Figure 1. Flowchart of the search procedure for the meta-analysis. CBM, China Biology Medicine; CNKI, China National
Knowledge Infrastructure; RCT, randomised controlled trial.

(1) ER (in 15 studies); (2) SFA (in nine studies), including results of the remaining 14 studies (RR 1.26, 95% CI 1.19
five scales: the water swallowing test41,42 (WST, three stud- to 1.34, n=14, P<0.001, fixed-effects model, details in
ies); videofluoroscopic swallowing study43 (VFSS, one online supplemntary appendix 1) and the forest plot of ER
study); standardised swallowing assessment44 (SSA, two (Figure 2A) suggested that, for patients with poststroke
studies); dysphagia outcome and severity scale45 (DOSS, dysphagia, a combination of acupuncture and swallowing
one study); and Fujishima Ichiro’s dysphagia scale46 (FDS, training yielded a higher ER than treatment with swallow-
two studies); (3) IA (MBI, one study); and (4) QOL ing training only. In the following subgroup and meta-
(S-QOL,47 two studies). Measurements of AEs, including regression analyses, no evidence of an influence of any
ecchymosis, haematoma, pain, mild vomiting, aspiration subgroup on the pooled ER was observed (all P>0.05,
pneumonia and malnutrition, were reviewed but not details in online supplemental appendix 2). In the analysis
included in the meta-analysis. The characteristics of the of publication bias, visual inspection of the funnel plot
included studies are shown in Table 1. Based on the (Figure 3A) and the use of metabias analysis (Begg’s and
Cochrane risk of bias tool and previous evaluation criteria, Egger’s tests) revealed significant publication bias (all
three studies were considered to be grade A. The quality P=0.001). Thus, a further trim-and-fill analysis and Nfs cal-
assessment is summarised in Table 2. culation were performed. The results showed that the
pooled estimated effect sizes after five iterations and the
addition of six missing studies were not significantly differ-
Synthesis of results ent before and after the trim-and-fill analysis (RR 1.27,
Effect size of ER. The ER data (15 studies, 1295 patients) 95% CI 1.21 to 1.33, Q=13.6, P=0.405; RR 1.22, 95% CI
were first analysed using a random-effects model. The 1.17 to 1.28, Q=29.5, P=0.059), and the filled funnel plot
pooled RR and 95% CI values showed significant heteroge- was approximately symmetrical (Figure 3B). Furthermore,
neity (I2=64.4%, n=15, P<0.001), which disappeared the fail-safe number (Nfs0.05=328.98; Nfs0.01=155.92) also
(I2=0.0%, n=14, P=0.857) after excluding one study.25 The indicated that there was no significant influence of

Acupuncture in Medicine, 37(2)


84

Table 1. Characteristics of the included studies.

Study Patients Interventions Designs Outcome

Duration (days,
ID First author Year Cases Age (years) weeks or months) MA (sessions) ST (sessions) E vs C Measures Conclusion

Acupuncture in Medicine, 37(2)


Ref. 24 Luo 2004 60 E, 60.50±6.21 E, 3.28±1.49m 28 28 in 4w MA+ST vs ST FDS Positive
C, 60.63±5.98 C, 3.22±1.41m

Ref. 25 Zhang 2007 220 E, 53.16±6.84 NR 30 30 in 1m MA+ST vs ST WST Positive


C, 51.37±8.63

Ref. 26 Zhang 2011 60 NR NR 30 24 in 4w MA+ST vs ST WST Positive

Ref. 27 Yu 2012 78 E, 63±10 E, 13.78±2.62d 20 20 MA+ST vs ST FDS Positive


C, 64±11 C, 14.56±2.48d

Ref. 28 Yi 2013 120 E, 61.0±6.5 E, 12.5±8.3d 30 90 in 1m MA+ST vs ST WST Positive


C, 59.2±7.3 C, 13.8±5.5d

Ref. 29 Yin 2013 113 E, 62.5±5.5 E, 11.5±2.2d 30 30 MA+ST vs ST SSA, S-QOL Positive
C, 60.8±7.4 C, 10.3±1.3d

Ref. 30 Li 2013 60 E, 56.9±4.6 NR 14 14 MA+ST vs ST WST Positive


C, 51.7±3.7

Ref. 31 Zhang 2014 60 E, 54.2±4.3 E, 3.9±0.5m 12 in 2w 12 in 2w MA+ST vs ST WST Positive


C, 53.7±2.9 C, 3.5±0.9m

Ref. 32 Tang 2014 96 E, 55.8±2.1 NR NR NR MA+ST vs ST WST Positive


C, 57.2±1.9

Ref. 33 Jia 2014 60 E, 58.30±7.87 <6m 24 in 4w 24 in 4w MA+ST vs ST WST Positive


C, 56.47±8.43
Acupuncture in Medicine
Li and Deng

Table 1. (Continued)
Study Patients Interventions Designs Outcome

Duration (days,
ID First author Year Cases Age (years) weeks or months) MA (sessions) ST (sessions) E vs C Measures Conclusion

Ref. 34 Liu 2014 87 E, 53.6±8.5 E, 2w−12m 14 14 MA+ST vs ST WST Positive


C C, 1w−11m

Ref. 35 Tong 2014 60 E, 63 E, 35 30 in 6w 30 in 6w MA+ST vs ST WST Positive


C, 62 C, 36 (D)

Ref. 36 Zhu FH 2015 60 E, 54.1±16.6 NR 14 14 MA+ST vs ST WST Positive


C, 49.5±22.7

Ref. 37 Zhu BB 2015 60 E, 53.60±12.96 E, 6.83±1.60m 28 28 in 4w MA+ST vs ST WST Positive


C, 56.10±10.81 C, 7.05±1.33m

Ref. 38 Fu 2016 101 E, 52.8±10.4 E, 6.8±2.3w 2m 2m MA+ST vs ST SSA Positive


C, 55.4±13.8 C, 8.5±3.1w

Ref. 39 Feng 2016 60 E, 60±12 E, 38±18d 18 in 3w 18 in 3w MA+ST vs ST VFSS Positive


C, 58±12 C, 39±18d

Ref. 40 Xia 2016 124 E, 65.3±14.2 E, 9.3±2.3d 24 in 4w 24 in 4w MA+ST vs ST DOSS, MBI, Positive
C, 66.1±14.3 C, 8.7±2.5d S-QOL

BP, bulbar palsy; C, control group; CH, cerebral haemorrhage; CI, cerebral ischaemia; d, day; DOSS, dysphagia outcome and severity scale; E, experimental group; FDS, Fujishima Ichiro’s dysphagia
scale (a 10-point scale for assessing dysphagia developed by Japanese scholar Fujishima Ichiro); ID, identity; m, month; MA; manual acupuncture; MBI, modified Barthel index; NR, not reported; PBP,
pseudobulbar palsy; SFA, swallowing function assessment; SH, subarachnoid haemorrhage; SSA, standardised swallowing assessment; ST, swallowing training; S-QOL, swallowing-related quality of life;
VFSS, videofluoroscopic swallowing study; w, week; WST, water swallow test (a five-grade scale for assessing dysphagia developed by Kubota Toshio, a Japanese scholar).

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86 Acupuncture in Medicine

Table 2. Methodological quality of the included studies.

Items

Blinding of Incomplete Grade of


Random sequence Allocation performance outcome Selective Other risk of
Study generation concealment and detection data reporting bias bias

Luo et al.24 L U U L L U B

Zhang et al.25 L U U L L U B

Zhang et al.26 L U L L L U A

Yu and Hu27 L U U L L U B

Yi28 L U U L L U B

Yin29 L U U L L U B

Li et al.30 L U U L L U B

Zhang31 L U U L L U B

Tang and Han32 L U U L L U B

Jia et al.33 L L U L L U A

Liu34 L U U L L U B

Tong et al.35 L U U L L U B

Zhu et al.36 L U U L L U B

Zhu and Zhao37 L U U L L U B

Fu38 L U U L L U B

Feng et al.39 L U U L L U B

Xia et al.40 L U L L L U A

L, low (risk of bias); H, high (risk of bias); U, unclear (risk of bias). A, four or more items meeting the ‘L’ level; B, two or three items meeting the ‘L’
level; C, one or no items meeting the ‘L’ level or one or more items meeting the ‘H’ level.

publication bias on the pooled effect size of ER (details in supplemental appendix 2), although the number of treat-
online supplemental appendix 3). ment sessions (<28 sessions vs ⩾28 sessions) yielded
different SMDs for SFA (<28 sessions: n=3; ⩾28 ses-
Effect size of SFA. The SFA data (nine studies, 776 eligible sions: n=2) with a significant difference between groups
patients) yielded positive results but with significant het- (P=0.004). By contrast, the meta-regression analyses
erogeneity (SMD 1.17, 95% CI 0.76 to 1.58, P<0.001; showed that the number of treatment sessions might not
I2=85.5%, n=9, P<0.001, online supplemental appendix influence the pooled effects of SFA (P=0.063). In the
1). The sensitivity analysis showed that four of the included following publication bias analysis, Begg’s funnel plot
studies28,31,33,38 were the primary contributors to the hetero- was visually symmetrical (Figure 3C), and no publica-
geneity; no substantial heterogeneity existed when these tion bias was observed in Begg’s and Egger’s tests
studies were excluded (SMD 1.40, 95% CI 1.18 to 1.61, (P=1.000 and P=0.869, respectively, online supplemen-
P<0.001; I2=53.8%, n=5, P=0.070, Figure 2B). Further- tal appendix 3).
more, the positive results were verified by the pooled
effect sizes of the excluded four studies but with heteroge- Effect size of IA. MBI data were extracted from one study40
neity (SMD 0.83, 95% CI 0.60 to 1.05, P<0.001; I2=91.1%, (with 124 eligible patients). The results showed that, com-
n=4, P<0.001, online supplemental appendix 1). Further pared with conventional swallowing training, combination
subgroup analysis was performed, and no study character- therapy might improve the activities of daily life in patients
istics were identified as potential influences of the hetero- with poststroke dysphagia (SMD 1.47, 1.07 to 1.87,
geneity of the estimated effect size (all P>0.05, online P<0.001; online supplemental appendix 1).

Acupuncture in Medicine, 37(2)


Li and Deng 87

Figure 2. Forest plots of effective rate, swallowing function assessment and swallowing-related quality of life. RR, relative risk;
SMD, standardised mean difference.

Effect size of QOL. S-QOL data were extracted from two Adverse events
studies,29,40 including 237 eligible patients, and negative
results were obtained in the meta-analysis (SMD 1.06, Data on AEs were collected from six studies.28,29,34,37–39 The
95% CI −0.04 to 2.17, P=0.06; Figure 2C, supplemental original results from the literature without statistics showed
appendices 1, 3). that the number of cases of aspiration pneumonia (32 in the

Acupuncture in Medicine, 37(2)


88 Acupuncture in Medicine

Figure 3. Funnel plots of effective rate and swallowing


Preferred acupuncture points
function assessment as a marker of publication bias analysis. We pooled the data related to the acupuncture points selected
RR, relative risk; SMD, standardised mean difference. from the included studies and found that nine acupuncture
points were most commonly used to treat dysphagia after
stroke: GB20, GB12 and TE17 in the nape; CV23 and Pang
Lianquan (0.8–1 cun from CV23) in the neck; and Jinjin,
Yuye and Yanhoubi (on the posterior pharyngeal wall) in the
mouth (online supplemental appendix 4). The findings were
similar to those of other published reviews.48,49

Discussion
Acupuncture and swallowing training are commonly used to
treat swallowing disorders in stroke patients as routine thera-
pies based on traditional Chinese medicine or modern
Western medicine. Furthermore, these therapies have been
used to treat other diseases, such as Parkinson’s disease.50
Whether the combination therapy has a more positive impact
on poststroke dysphagia than conventional swallowing train-
ing remains unclear. To our knowledge, this is the first meta-
analysis to evaluate the effectiveness and safety of the
combination of acupuncture and swallowing training versus
conventional care for treating poststroke dysphagia. Previous
studies have provided limited evidence due to small sample
sizes and poor methodological quality. Therefore, in the pre-
sent study, a meta-analysis with rigorous inclusion criteria
for RCTs (only RCTs that clearly stated use of random
sequence generation were included) were defined to provide
a reliable quantitative evaluation of existing evidence on the
effectiveness and safety of acupuncture and swallowing
training for the treatment of poststroke dysphagia. To com-
prehensively assess the value of acupuncture combined with
swallowing training, data on SFA, IA and QOL were chosen
to evaluate for improvements in multiple dimensions among
patients with poststroke dysphagia. Moreover, the ER was
taken as a global measure of clinical effectiveness. In the
meta-analysis, the estimated effect sizes of ER, SFA, MBI
and QOL suggested that the combined application of acu-
puncture and swallowing training improved swallowing
function and activities of daily life to a significantly greater
degree, than swallowing training alone. The negative result
regarding QOL might be due to the small number of included
studies and the small number of eligible patients. Overall,
the effectiveness and safety of acupuncture and swallowing
training for patients with poststroke dysphagia were con-
experimental group and 39 in the control group), malnutri- firmed by this meta-analysis. Regarding acupuncture points,
tion (two cases in the control group) and dehydration (four we summarised nine preferred points based on the included
cases in the experimental group and five cases in the con- studies and thereby provide recommendations for clinical
trol group) were higher in the control group than in the and research settings.
experimental group (online supplemental appendix 4).
Additionally, AEs related to acupuncture, such as pain,
Limitations
mild vomiting, ecchymosis and haematoma, occurred
rarely and were not severe. No AEs related to swallowing There were some limitations in the present study. First, sub-
training were reported in the included studies. stantial heterogeneity and publication bias were observed

Acupuncture in Medicine, 37(2)


Li and Deng 89

in the included studies for the pooled estimation of the ER. 4. Wieseke A, Bantz D, Siktberg L, et al. Assessment and early diagnosis
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