Effectiveness of Non invasive Brain Stim

  Effectiveness of Non-invasive Brain Stimulation in Dysphagia Subsequent

to Stroke: A Systemic Review and Meta-

analysis

Seung Nam Yang, Sung-Bom Pyun, Hyun Jung Kim, Hyeong Sik Ahn & Byung Joo Rhyu Dysphagia

  Dedicated to advancing the art and science of deglutology

  ISSN 0179-051X Dysphagia DOI 10.1007/s00455-015-9619-0

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  Effectiveness of Non-invasive Brain Stimulation in Dysphagia Subsequent to Stroke: A Systemic Review and Meta-analysis

  = 72 %). A subgroup analysis based on the type of intervention (three repetitive tran- scranial magnetic stimulation (rTMS) studies and three transcranial direct current stimulation (tDCS) studies) re- vealed a statistically significant beneficial effect of NIBS compared with sham stimulation in the rTMS group, but not in the tDCS group. When the results were examined based on intervention site (ipsilesional vs. contralesional site stimulation), no statistically significant difference was noted between two groups. No complications of NIBS were reported in this analysis.

  NIBS involves repetitive & Sung-Bom Pyun rmpyun@korea.ac.kr & Hyun Jung Kim moole02@naver.com 1 Department of Physical Medicine and Rehabilitation, Korea University College of Medicine, 73 Inchon-ro, Seongbuk-gu,

  NIBS is a method used to modulate human brain func- tion. In NIBS, a given neuron uses several different neu- rotransmitters to regulate a diverse population of central nervous system neurons [

   ].

  majority of patients spontaneously recover from dysphagia, various life-threatening complications, such as aspiration pneumonia, asphyxia, and malnutrition, can occur ]. Currently used treatment methods for dysphagia after stroke include posture training, dietary modifications, swallowing exercises, drug therapy, oromotor stimulation, neuromuscular electrical stimulation, non-invasive brain stimulation (NIBS), and botulinum toxin injection [

  Although the

  Dysphagia is a major complication subsequent to cere- brovascular disease. The prevalence of dysphagia follow- ing stroke varies from 27 to 64 % [

  Introduction

  Transcranial direct current stimulation Meta-analysis

  Keywords Deglutition disorders Cerebrovascular disorders Transcranial magnetic stimulation

  2

  Seung Nam Yang

  Abstract The objective of this study is to assess the ef- ficacy and safety of non-invasive brain stimulation (NIBS) in patients with dysphagia subsequent to stroke. A sys- tematic search of the literature published by Medline (January 1, 1976 through June 21, 2013), EMBASE (Jan- uary 1, 1985 through June 21, 2013), and the Cochrane Library (January 1, 1987 through June 21, 2013) was conducted for all relevant articles related to NIBS, dys- phagia, and cerebrovascular disorders (CVD). Two re- viewers (S.N.Y and S.B.P) independently evaluated the eligibility of retrieved data according to the selection cri- teria and assessed methodological quality of the studies using the ‘assessing risk of bias’ table recommended in the Cochrane Handbook for Systematic Reviews of Interven- tions (version 5.0.2). Six randomized controlled trials (59 intervention groups and 55 placebo groups) were identified as addressing the use of NIBS for dysphagia after CVD and were included in the meta-analysis. The function scale score improvement of dysphagia in patients treated with NIBS was statistically significant compared with that of patients who underwent sham stimulation (standardized mean difference = 1.08, 95 % confidence intervals = 0.29–1.88, p = 0.008; I

  Ó Springer Science+Business Media New York 2015

  Byung Joo Rhyu

  2

  Hyeong Sik Ahn

  

2

  Hyun Jung Kim

  1

  Sung-Bom Pyun

  1

  Seoul 136-705, South Korea 2 Department of Preventive Medicine, Korean University College of Medicine, 73 Inchon-ro, Seongbuk-gu, Seoul 136-705, South Korea 3 Department of Physical Medicine and Rehabilitation, Sahmyook Medical Center, Seoul, South Korea Dysphagia DOI 10.1007/s00455-015-9619-0 transcranial magnetic stimulation (rTMS) and transcranial direct current stimulation (tDCS). rTMS is a non-invasive stimulation technique that allows for the focal depolariza- tion of neurons in targeted cortical areas by changing magnetic fields below the skull. This technique can activate or suppress activity in cortical regions depending on the frequency applied [

  tDCS is an additional NIBS

  Data Extraction Process and Data Items All the data were extracted from the studies by one author (S.N.Y) using a structured form; data were checked by another author (S.B.P). The following variables were extracted: (1) the mean and standard deviation (SD) of the dysphagia outcome score before and at follow-up for the intervention and control groups; (2) demographic, clinical, and treatment characteris- tics (e.g., the number of patients in the intervention and control groups as well as the participants’ age, gender, and baseline characteristics); (3) intervention protocol type; (4) rTMS and tDCS stimulation parameters (region of stimulation site, the total number of stimulation, the method and duration of stimulation); and (5) the assessment method. If important data were not presented in the paper, we contacted the data from the author by email to request the data. Assessment of Methodological Quality The methodological qualities of the included studies were also assessed independently by S.N.Y and S.B.P. RCTs were assessed using a seven-item scale of risk of bias scale developed by the Cochrane Bias Method Group. The five bias scores assessed include selection, performance, attri- tion, detection, and reporting biases. Disagreements be- tween reviewers were resolved through discussion or review by the third author.

  S. N. Yang et al.: Effectiveness of Non-invasive Brain Stimulation in Dysphagia Subsequent

  We conducted a meta-analysis to pool these outcomes across the included studies, estimating the change from the baseline (pre-stimulation) for the different severity levels of dysphagia treated with NIBS and their associated 95 % confidence intervals. Two studies presented data in image form, which we measured and converted to numeric values.

  ofluoroscopic Dysphagia Scale ].

  and the Vide-

  the Functional Dysphagia Scale [

   ],

  Main and Subgroup Analyses The main analysis involved the association between NIBS and dysphagia evaluation. Four types of dysphagia evaluation were used: the Dysphagia Outcome and the Severity Scale (four-point and seven-point scales)

  Selection Criteria We included trials that met the following four criteria: (1) trials assessing adult patients (male or female [18 years of age) with a history of CVD; (2) patients had dysphagia and received NIBS such as rTMS or tDCS; (3) the study was an RCT; and (4) the study reported outcome measures for dysphagia. Two reviewers (S.N.Y and S.B.P) indepen- dently evaluated the eligibility of all the retrieved data based on the selection criteria.

  technique that uses a weak direct current to modulate the activation of sodium- and calcium-dependent channels and NMDA receptor activity and enhance or depress ex- citability depending on the duration and polarity of stimulation [

  or recently completed trials. The research was performed without restrictions regarding language or year of publi- cation. The articles cited in the reference lists of included articles were also manually searched.

   ) for trial registrations to identify ongoing

  We used multiple comprehensive databases to identify literature on the efficacy of NIBS on dysphasia. This study is based on the Cochrane Review Methods ]. Literature Search We searched Medline (January 1, 1976 through June 21, 2013), EMBASE (January 1, 1985 through June 21, 2013), and the Cochrane Library (January 1, 1987 through June 21, 2013). The following medical subject headings (MeSH) and keywords were searched through Medline: cere- brovascular disorders (CVD), basal ganglia cerebrovascu- lar disease, brain ischemia, intracranial aneurysm, intracranial arterial diseases, intracranial embolism and thrombosis, intracranial hemorrhages, stroke, electric stimulation therapy, transcranial magnetic stimulation, and deglutition disorders. Additional search terms included swallowing disorders, dysphagia, oropharyngeal dyspha- gia, esophageal dysphagia, swallowing, tDCS, and rTMS. The search strategies adapted for the other databases were based on the MEDLINE strategy. After the initial elec- tronic search, we used the highly sensitive Cochrane RCT filter to exclude non-randomized control trials. We also searched an international database

  The objective of this study was to use a meta-analysis of randomized controlled trials (RCTs) to investigate the ef- ficacy and safety of NIBS for treating dysphagia subse- quent stroke.

  

  numerous post-stroke rehabilitation fields, including motor impairment, aphasia, and impaired cognition. Recently, a positive effect of NIBS on dysphagia after stroke was re- ported

  NIBS is increasingly been used in

Methods

  However, these values indicated the values at baseline and after treatment and not the change from the baseline. Thus, we estimated the SD using the correlation coefficient of each group, which was derived from the included studies. We performed the subgroup analysis based on the NIBS method (rTMS or tDCS) and the stimulation site (con- tralesional vs. ipsilesional site stimulation). Statistical Analysis All statistical analyses were performed with Reviewer Manager Software 5.0 (Cochrane Collaboration, Oxford, UK). A statistical analysis for continuous variables was performed. To estimate heterogeneity, we used I

  stroke (approximately 1 week after stroke). The other studies included subjects in the subacute stage (ap- proximately 1–3 months after stroke). Different therapeutic outcomes were evaluated in each study. Four subscales of the Dysphagic Outcome and Severity Scale [

  the contralesional side of the brain, and three other studies (Khedr et al.

  and Shigematsu et al.

  

   ] ) stimulated the ipsilesional side of the brain. The

  study by Khedr et al. [

  stimulated either or both hemi-

  spheres. In these studies, patients in the acute and subacute stages of stroke were included. The subjects in Kumar et al.

   ] were in the acute stage of

  were used

  evaluated the effect of tDCS compared with sham stimulation, and the other three studies evaluated the effect of rTMS compared with sham stimulation. All the studies were conducted to stimulate the brain by enhancing ac- tivity, such as anodal stimulation in tDCS or high-fre- quency stimulation (3–5 Hz) in rTMS. However, two studies (Kumar et al. [

  in the two studies by Khedr et al. [

   ], and seven

  subscales of the Dysphagia Outcome and Severity Scale

  and

  Shigematsu et al. [

  and

  Park et al.

  

  and Videofluoroscopic Dysphagia Scale ], respectively.

   ]) stimulated

  Three studies

  2

  Because no consistent scale was used to assess swal- lowing function across studies, we pooled the data using the change from baseline across groups. The outcomes were expressed as the standardized mean difference with 95 % confidence intervals.

  , which measures the percentage of total variation across trials. I

  2

  was calculated as follows: 100.0 % 9 (Q - df)/Q, where Q is the Cochran heterogeneity measure. Negative I

  2

  values were defined as 0 such that I

  2

  ranged between 0.0 % (no observed heterogeneity) and 100.0 % (maximal hetero- geneity). An I

  2

  value greater than 50.0 % was considered to be substantial heterogeneity. When significant heterogeneity existed, a random effects model was used for the analysis; otherwise, a fixed effects model was used.

  Tests for funnel plot asymmetry are generally only performed when at least 10 studies are included in the meta-analysis. Given that our analysis only includes six studies, tests for asymmetry would be ineffective because they could not differentiate chance from asymmetry.

  of the six RCTs. We evaluated the risk of bias for the six studies using Cochrane Collaboration guidelines; the re- sults are presented in the ‘Characteristics of the included studies’ tables and summarized in Fig.

  Results

  Study Selection Figure

   illustrates how relevant RCTs were identified for

  the final analysis. A total of 136 articles were retrieved by searching three databases and reviewing relevant bibliogra- phies. We excluded 37 duplicate articles and an additional 71 articles that did not fulfill the selection criteria. After re- viewing the full text of the remaining 28 articles, we ex- cluded 22 articles for several reasons, as presented in Fig.

  

  

   ]. Six RCTs met the inclusion criteria and were included in the systematic review and meta-analysis.

  Study Characteristics Of the six included studies, two were conducted in Egypt, two in South Korea, one in the US, and one in Japan. These included trials were reported between March 2009 and April 2013. Table

   summarizes the general characteristics

  Fig. 1 Flow chart summarizing the selection process S. N. Yang et al.: Effectiveness of Non-invasive Brain Stimulation in Dysphagia Subsequent Table 1 Characteristics of the studies of non-invasive brain stimulation treatment for dysphagia after stroke Author, year (country) Participants Mean age of participants

  (years) Intervention vs. control Stimulation site Duration of treatment Main outcome Time after stroke

  Anodal tDCS (1 mA for 20 min) or sham (1 mA for 30 s) stimulation with a 2-surface electrode

  N. Yang et al.: Effectiveness of Non-invasive Brain Stimulation in Dysphagia Subsequent

  Outcome Severity Scale (7 points) 5–38 (12.5 ± 8.0) weeks after onset rTMS repetitive transcranial magnetic stimulation, tDCS transcranial direct current stimulation, FDI first dorsal interosseous muscle, s second, min minute S.

  Anodal tDCS or sham stimulation of 1 mA with a 2-surface electrode Ipsilesional hemisphere 20 min for 10 days Dysphagia

   ] 20 patients with dysphagia related to stroke 65.8 ± 8.0

  Shigematsu et al. 2013 (Japan) [

  45–91(59.9 ± 16.3) days after onset Control groups 36–114(63.9 ± 26.3) days after onset

  Videofluoroscopic Dysphagia Scale (100 points) Intervention

  10 sessions of 5 Hz for 10 s/min for 10 min for 10 days

  5 Hz stimulation at 90 % of the thenar motor threshold Contralesional hemisphere, pharyngeal hot spot

  71.3 ± 7.3 rTMS or sham stimulation for

   ] 18 patients with dysphagia related to unilateral hemisphere stroke

  2013 (Republic of Korea) [

  (100 points) 25.9 ± 10.2 days after onset within 2 months after onset Park et al.

  Ipsilesional hemisphere 20 min for 10 days Functional Dysphagia Scale

   ] 14 patients with dysphagia related to unilateral hemispheric infarction 71.0 ± 10.8

  Khedr et al.

  2012 (Republic of Korea) [

  Yang et al.

  Outcome Severity Scale (7 points) 1–7 days after onset

  The contralesional sensory and motor cortical area for swallowing 30 min for 5 days Dysphagia

  74.9 ± 11.8 Anodal tDCS or sham stimulation 2 mA with a 2-surface electrode

  2011 (USA) [ ] 14 patients with dysphagia related to unilateral hemispheric infarction

  Outcome and Severity Scale (4 points) 1–3 months after onset Kumar et al.

  3 Hz stimulation at 130 % of the resting motor threshold of FDI Both esophageal cortical areas 10 sessions of 3-Hz stimulation for 10 s/min for 10 min for 5 days Dysphagic

  2010 (Egypt) [ ] 22 patients with dysphagia related to brain stem infarction 56.4 ± 15 for 11 lateral medullar infarction 58.2 ± 10.4 for 11 other brain infarction rTMS or sham stimulation for

  5–10 days after onset Khedr et al.

  Dysphagic Outcome and Severity Scale (4 points)

  Ten sessions of 3-Hz stimulation for 10 s/min for 10 min for 5 days

  3 Hz stimulation at 120 % of the resting motor threshold of FDI Fig. 8 coil Either the ipsilesional or the contralesional esophageal cortical area

  2009 (Egypt) [ ] 26 patients with dysphagia related to monohemi- spheric stroke 57.3 ± 12.5 rTMS or sham stimulation for

  123

  Both tools are similar 100-point scales based on the find- ings of a videofluoroscopic swallowing study performed by the same research group (Table ).

  I

  nificant improvement that appeared to become more pro- nounced over time compared with the sham stimulation

  after stimulation revealed statistically sig-

  2 = 0 %; Fig.

  I

  ence = 3.54, 95 % confidence intervals = 2.58–4.50,

  and 2 months (standardized mean differ-

  2 = 70 %; Fig.

  evaluations at 1 month (standardized mean differ- ence = 2.75, 95 % confidence intervals = 1.47–4.04,

  All the RCTs included in this review reported that NIBS had a positive effect on post-stroke dysphagia. In the two articles by Khedr et al.

  The results of the

  2 = 72 %; Fig.

  between the two groups (real vs. sham rTMS). They compared the dysphagia scores before and immediately after stimulation as well as before and 4 weeks after stimulation in the rTMS group and control group using the Wilcoxon signed rank test. We asked those authors for the difference in the dysphagia scores before and immediately after stimulation (real vs. sham rTMS) and used these data in our meta-analysis. Meta-analysis and the Effects of NIBS In the meta-analysis of the six studies, statistically significant improvement was noted in patients with dysphagia who were treated with NIBS immediately after stimulation compared with the patients who underwent sham stimulation (stan- dardized mean difference = 1.08, 95 % confidence inter- vals = 0.29–1.88, I

   ] did not report the change in the dysphagia outcome

  after stimulation in the tDCS group compared with the control group. They reported no significant difference immediately after stimulation (real vs. sham tDCS). They did not include the numeric values for the changes between before and im- mediately after stimulation in their article. We asked the au- thors for the dysphagia outcome values immediately after stimulation and used these data in the meta-analysis. Park et al.

   ] reported statistically significant improvement 3 months

  before as well as immediately, 1 month, and 2 months after stimulation; however, the authors did not report the statistical change in dysphagia outcomes at any of these time points. Two-factor repeated-measures analysis of variance (ANOVA) was used to compare the differential effects of the rTMS conditions (real vs. sham rTMS) on changes in the dysphagia rating, with treatment (real vs. sham rTMS) and time (before vs. after treatment) as the main factors. Yang et al.

   ], the outcomes were measured

  Fig. 2 Risk of bias assessment for six trials S. N. Yang et al.: Effectiveness of Non-invasive Brain Stimulation in Dysphagia Subsequent

  … S. N. Yang et al.: Effectiveness of Non-invasive Brain Stimulation in Dysphagia Subsequent

  

Fig. 3 Forest plot of the subset of studies with data available for a systematized comparison of non-invasive brain stimulation for dysphagia after

stroke Fig. 4 Forest plot of the subgroup analysis of the intervention

  group. An analysis of subgroups based on intervention use significant improvement compared with the sham stimulation revealed significant improvement in the rTMS group vs. the group (standardized mean difference = 0.90, 95 % confi-

  2

  sham stimulation group (standardized mean differ-

  whereas the dence intervals = 0.16–1.64, I = 0 %; Fig.

  95 % confidence ipsilesional site stimulation group did not exhibit improve- ence = 1.61, intervals = 0.59–2.63,

  2 ). However, no statistically significant dif-

  I = 67 %; Fig. ment (standardized mean difference = 1.015, 95 % confi-

  2

  ference was observed in the tDCS group vs. the sham dence I Fig.

  

  intervals = -0.69–2.79, = 88 %; However, no statistically significant difference was noted stimulation group (standardized mean difference = 0.54,

  2

  95 % confidence I between the ipsilesional stimulation group and the contrale- intervals = -0.05–1.62, = 68 %;

  2 Fig. ). No = 0 %, p = 0.87; Fig.

  the contralesional site stimulation group exhibited statistically complications of NIBS were reported in these studies.

Discussion

   ]. At present, we cannot draw conclusions regarding

  Fig. 5 Forest plot of the subgroup analysis of the stimulation site S. N. Yang et al.: Effectiveness of Non-invasive Brain Stimulation in Dysphagia Subsequent

  There are several limitations to this review. The number of included studies and the sample size of each study were small. Although the Egger’s test results indicated that the small-study effect did not exist (p = 0.919), the results of this study are of limited value. However, because Egger’s

  tDCS and rTMS that were included in this analysis, in- sufficient data were available to determine the effects of those techniques on dysphagia. However, it may be con- cluded that acupuncture and behavioral therapies may re- duce symptoms of dysphagia. Based on the Cochrane reviews, it can also be concluded that, although percuta- neous endoscopic gastrostomy results in fewer treatment failures compared with nasogastric tube feeding, it is not superior to nasogastric feeding.

   ]. Given the small number of studies regarding

  NIBS was included as an intervention for dysphagia in Cochrane reviews (2012) related to dysphagia intervention and nutritional support in acute and subacute stroke pa- tients

  which type of site stimulation is more beneficial.

  This systematic review provides an overview of currently available evidence for the use of NIBS in dysphagia sub- sequent to stroke. The results suggest that NIBS improves swallowing in stroke patients. Subgroup analyses revealed a beneficial effect in the rTMS group that was not observed in the tDCS group. No significant difference between the different stimulation sites (ipsilesional or contralesional stimulation) was observed. The six studies included in the meta-analysis exhibited significant heterogeneity with re- spect to dysphagia assessments, study population, stroke etiology, stroke characteristics, and the time to intervention after stroke onset.

  In our analysis, NIBS application exhibited synergistic effects over time, i.e., the intervention effect was more beneficial 1–2 months after the intervention compared with immediately after the intervention. However, the general- izability of present findings may be restricted by the limited number of long-term follow-up studies that have been conducted.

   ]. Thus,

  In all these studies, enhancing mode was used for stimulation to the brain. However, the brain stimulation sites differed among the studies. Swallowing musculature is represented in bilateral hemispheres [

  follow-up outcome measures at 3 months and synergistic effects over time.

  reported improved

  obtained immediately after intervention differed from the results of other studies. The differences in the study population characteristics and the intervention and evaluation methods were not unique, and we could not provide a reason for these differences in results. However, similar to other studies, Yang et al. [

  

  In this meta-analysis, the results that Yang et al. [

  stimulation of either the ipsilesional or the contralesional hemisphere is theoretically reasonable. Subgroup analyses revealed that the intervention effects were beneficial only in the contralesional stimulation group. Such effects were not observed in the ipsilesional group. However, the mean standard difference for the ipsilesional stimulation group (1.05) was greater than that of the contralesional stimula- tion group (0.90). Given the heterogeneity of ipsilesional stimulation and its wide confidence intervals, neuro- modulation with contralesional stimulation was not effec- tive compared with sham stimulation. Additionally, the confidence intervals of the two subgroups overlapped (ipsilesional site [-0.69–2.79] vs. contralesional site [0.16–1.64]), and the differences were not statistically significant. In addition, dysphagia studies that used bilat- eral cortical stimulation were also reported, currently [ test is commonly known to have limited effectiveness for studies involving fewer than 10 trials, we did not include this result in our study. Given the various swallowing scales used in the included studies, the standardized mean difference was chosen as the measure of effectiveness. Additionally, we analyzed the differences in outcome for real vs. sham stimulation only immediately after stimula- tion because this time point exclusively provided consistent data. Therefore, the long-term outcome after NIBS could not be evaluated. The effect of NIBS on dysphagia pre- sented in these studies was not evaluated according to brain plasticity assessments such as imaging tests but according to clinical evaluation. The assessment of changes in brain plasticity resulting from NIBS was suggested as future research topic.

  Conclusions

  18. Park JW, Oh JC, Lee JW, Yeo JS, Ryu KH. The effect of 5 Hz high- frequency rTMS over contralesional pharyngeal motor cortex in post-stroke oropharyngeal dysphagia: a randomized controlled study. Neurogastroenterol Motil. 2013;25(4):324-e250.

  13. Gandiga PC, Hummel FC, Cohen LG. Transcranial DC stimulation (tDCS): a tool for double-blind sham-controlled clinical studies in brain stimulation. Clin Neurophysiol. 2006;117(4):845–50.

  14. Khedr EM, Abo-Elfetoh N. Therapeutic role of rTMS on recovery of dysphagia in patients with lateral medullary syndrome and brainstem infarction. J Neurol Neurosurg Psychiatry. 2010;81(5):495–9.

  15. Khedr EM, Abo-Elfetoh N, Ahmed MA, Kamel NF, Farook M, El Karn MF. Dysphagia and hemispheric stroke: a transcranial magnetic study. Neurophysiol Clin. 2008;38(4):235–42.

  16. Khedr EM, Abo-Elfetoh N, Rothwell JC. Treatment of post- stroke dysphagia with repetitive transcranial magnetic stimula- tion. Acta Neurol Scand. 2009;119(3):155–61.

  17. Shigematsu T, Fujishima I, Ohno K. Transcranial direct current stimulation improves swallowing function in stroke patients.

  Neurorehabil Neural Repair. 2013;27(4):363–9.

  19. Yang EJ, Baek SR, Shin J, Lim JY, Jang HJ, Kim YK, et al.

  12. Kumar S, Wagner CW, Frayne C, Zhu L, Selim M, Feng W, et al.

  Effects of transcranial direct current stimulation (tDCS) on post- stroke dysphagia. Restor Neurol Neurosci. 2012;30(4):303–11.

  20. Higgins JPT, Green S. Cochrane collaboration: cochrane hand- book for systematic reviews of interventions. Chichester, Hobo- ken: Wiley; 2008.

  21. Parker C, Power M, Hamdy S, Bowen A, Tyrrell P, Thompson DG. Awareness of dysphagia by patients following stroke pre- dicts swallowing performance. Dysphagia. 2004;19(1):28–35.

  22. O’Neil KH, Purdy M, Falk J, Gallo L. The dysphagia outcome and severity scale. Dysphagia. 1999;14(3):139–45.

  23. Han TR, Paik NJ, Park JW. Quantifying swallowing function after stroke: a functional dysphagia scale based on videofluoro- scopic studies. Arch Phys Med Rehabil. 2001;82(5):677–82.

  24. Han TR, Paik NJ, Park JW, Kwon BS. The prediction of per- sistent dysphagia beyond six months after stroke. Dysphagia.

  Noninvasive brain stimulation may improve stroke-related dys- phagia: a pilot study. Stroke. 2011;42(4):1035–40.

  11. Hallett M. Transcranial magnetic stimulation and the human brain. Nature. 2000;406(6792):147–50.

  We performed a systematic review and meta-analysis of RCTs that investigated the beneficial effects of NIBS on dysphagia. Our results indicate that NIBS treatment for dysphagia after stroke has a beneficial effect compared with sham stimulation. Moreover, NIBS reveals synergistic effects over time. In the subgroup analysis, rTMS stimulation offered beneficial effects compared with sham stimulation. No significant difference according to stimulation site (ipsilesional or contralesional stimulation) was noted. No complications from NIBS were reported in this analysis. The small number of studies and the lack of long-term follow-up are major limitations of this review. Future studies would benefit from the standardization of outcomes and stimulation parameters to decrease the variability and heterogeneity of the results and the long- term outcomes.

  4. Smithard DG, O’Neill PA, Parks C, Morris J. Complications and outcome after acute stroke. Does dysphagia matter? Stroke.

  Conflict of interest The authors have no conflict of interest to disclose.

  Disclosure All authors have no substantial direct or indirect com- mercial financial incentive associated with publishing this article. All authors had full access to all of the data used in the study and take responsibility for the integrity of the data and the accuracy of the data analysis.

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PENGARUH PENERAPAN MODEL DISKUSI TERHADAP KEMAMPUAN TES LISAN SISWA PADA MATA PELAJARAN ALQUR’AN HADIS DI MADRASAH TSANAWIYAH NEGERI TUNGGANGRI KALIDAWIR TULUNGAGUNG Institutional Repository of IAIN Tulungagung

119 3984 16

PENGARUH PENERAPAN MODEL DISKUSI TERHADAP KEMAMPUAN TES LISAN SISWA PADA MATA PELAJARAN ALQUR’AN HADIS DI MADRASAH TSANAWIYAH NEGERI TUNGGANGRI KALIDAWIR TULUNGAGUNG Institutional Repository of IAIN Tulungagung

40 1057 43

PENGARUH PENERAPAN MODEL DISKUSI TERHADAP KEMAMPUAN TES LISAN SISWA PADA MATA PELAJARAN ALQUR’AN HADIS DI MADRASAH TSANAWIYAH NEGERI TUNGGANGRI KALIDAWIR TULUNGAGUNG Institutional Repository of IAIN Tulungagung

40 945 23

PENGARUH PENERAPAN MODEL DISKUSI TERHADAP KEMAMPUAN TES LISAN SISWA PADA MATA PELAJARAN ALQUR’AN HADIS DI MADRASAH TSANAWIYAH NEGERI TUNGGANGRI KALIDAWIR TULUNGAGUNG Institutional Repository of IAIN Tulungagung

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PENGARUH PENERAPAN MODEL DISKUSI TERHADAP KEMAMPUAN TES LISAN SISWA PADA MATA PELAJARAN ALQUR’AN HADIS DI MADRASAH TSANAWIYAH NEGERI TUNGGANGRI KALIDAWIR TULUNGAGUNG Institutional Repository of IAIN Tulungagung

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KREATIVITAS GURU DALAM MENGGUNAKAN SUMBER BELAJAR UNTUK MENINGKATKAN KUALITAS PEMBELAJARAN PENDIDIKAN AGAMA ISLAM DI SMPN 2 NGANTRU TULUNGAGUNG Institutional Repository of IAIN Tulungagung

60 1348 14

KREATIVITAS GURU DALAM MENGGUNAKAN SUMBER BELAJAR UNTUK MENINGKATKAN KUALITAS PEMBELAJARAN PENDIDIKAN AGAMA ISLAM DI SMPN 2 NGANTRU TULUNGAGUNG Institutional Repository of IAIN Tulungagung

66 1253 50

KREATIVITAS GURU DALAM MENGGUNAKAN SUMBER BELAJAR UNTUK MENINGKATKAN KUALITAS PEMBELAJARAN PENDIDIKAN AGAMA ISLAM DI SMPN 2 NGANTRU TULUNGAGUNG Institutional Repository of IAIN Tulungagung

20 825 17

KREATIVITAS GURU DALAM MENGGUNAKAN SUMBER BELAJAR UNTUK MENINGKATKAN KUALITAS PEMBELAJARAN PENDIDIKAN AGAMA ISLAM DI SMPN 2 NGANTRU TULUNGAGUNG Institutional Repository of IAIN Tulungagung

32 1111 30

KREATIVITAS GURU DALAM MENGGUNAKAN SUMBER BELAJAR UNTUK MENINGKATKAN KUALITAS PEMBELAJARAN PENDIDIKAN AGAMA ISLAM DI SMPN 2 NGANTRU TULUNGAGUNG Institutional Repository of IAIN Tulungagung

41 1350 23