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Respiratory Muscle Training Reduces Respiratory Complications and Improves Swallowing Function After Stroke: A Systematic Review and Meta-Analysis

Open AccessPublished:November 12, 2021DOI:https://doi.org/10.1016/j.apmr.2021.10.020

      Abstract

      Objective

      To investigate whether respiratory muscle training is capable of reducing the occurrence of respiratory complications and improving dysphagia (swallowing or cough function) after stroke.

      Data Sources

      Cochrane Library, Excerpta Medical Database (EMBASE), PUBMED, and Web of Science were searched for studies published in English; the China Biology Medicine (CBM), China Science and Technology Journal Database (VIP), China National Knowledge Infrastructure (CNKI), and Wanfang Database were searched for studies published in Chinese up to August 10, 2021.

      Study Selection

      Eleven randomized control trials (RCTs) (N=523) met the inclusion criteria were included in this systematic review.

      Data Extraction

      Data and information were extracted by two reviewers independently and disagreements was resolved by consensus with a third coauthor. Primary outcome was the occurrence of respiratory complications, secondary outcomes would be represented by swallowing and cough function. The quality of each included RCT were assessed by Cochrane risk-of-bias criteria and the GRADE evidence profile was provided to present information about the body of evidence and judgments about the certainty of underlying evidence for each outcome.

      Data Synthesis

      Respiratory muscle training reduced the risk of respiratory complications (relative risk, 0.51; 95% confidence interval [CI], 0.28-0.93; I2=0%; P=.03; absolute risk difference, 0.068; number need to treat, 14.71) compared with no or sham respiratory intervention. It also decreased the liquid-type Penetration-Aspiration Scale scores by 0.81 (95% CI, –1.19 to –0.43; I2=39%; P<.0001). There was no significant association between respiratory muscle training and Functional Oral Intake Scale (FOIS) scores, cough function: increased FOIS scores by 0.47 (95% CI, –0.45 to 1.39; I2=55%; P=.32), decreased peak expiratory cough flow of voluntary cough by 18.70 L per minute (95% CI, –59.74 to 22.33; I2=19%; P=.37) and increased peak expiratory cough flow of reflex cough by 0.05 L per minute (95% CI, –40.78 to 40.87; I2=0%; P>.99).

      Conclusion

      This meta-analysis provided evidence that respiratory muscle training is effective in reducing the risk of respiratory complications and improving dysphagia by reducing penetration or aspiration during swallowing liquid bolus after stroke. However, there was no sufficient evidence to determine that respiratory muscle training improves cough function. Additional multicenter studies using larger patient cohorts are required to validate and support these findings. Furthermore, long-term follow-up studies should be performed to measure outcomes, while avoiding bias due to confounding factors such as heterogeneity of the etiologies of dysphagia.

      Keywords

      List of abbreviations:

      CI (confidence interval), CVA (cough volume acceleration), FOIS (Functional Oral Intake Scale), PAS (Penetration-Aspiration Scale), PECF-RC (peak expiratory cough flow of reflex cough), PECF-VC (peak expiratory cough flow of voluntary cough), RCT (randomized controlled trial), RR (relative risk)
      Dysphagia is a very common complication observed in stroke patients. The incidence rate is highly variable. It is lowest when identified using screening methods (ie, the water swallow test), with an incidence of approximately 37% to 45%, whereas it is highest when identified using instrumental testing (ie, videofluoroscopy), with an incidence rate of approximately 64% to 78%.
      • Martino R
      • Foley N
      • Bhogal S
      • Diamant N
      • Speechley M
      • Teasell R.
      Dysphagia after stroke: incidence, diagnosis, and pulmonary complications.
      Aspiration is associated with an 11-fold increase in the risk of chest infections or pneumonia,
      • Martino R
      • Foley N
      • Bhogal S
      • Diamant N
      • Speechley M
      • Teasell R.
      Dysphagia after stroke: incidence, diagnosis, and pulmonary complications.
      which is one of the most troublesome respiratory complications after stroke and may result in death.
      • Hannawi Y
      • Hannawi B
      • Rao CPV
      • Suarez JI
      • Bershad EM.
      Stroke associated pneumonia: major advances and obstacles.
      Using pooled analysis from studies with sufficient data, the risk of pneumonia was found to be increased in patients with dysphagia, especially in patients with aspiration (relative risk [RR], 11.56; 95% confidence interval [CI], 3.36-39.77).
      • Martino R
      • Foley N
      • Bhogal S
      • Diamant N
      • Speechley M
      • Teasell R.
      Dysphagia after stroke: incidence, diagnosis, and pulmonary complications.
      Furthermore, patients who develop pneumonia have higher mortality rates, longer hospitalization, poorer functional outcomes, and higher care needs.
      • Hannawi Y
      • Hannawi B
      • Rao CPV
      • Suarez JI
      • Bershad EM.
      Stroke associated pneumonia: major advances and obstacles.
      ,
      • Finlayson O
      • Kapral M
      • Hall R
      • et al.
      Risk factors, inpatient care, and outcomes of pneumonia after ischemic stroke.
      Although some studies have reported that approximately 90% of patients with dysphagia usually improve spontaneously with a return of safe swallowing function within 2 weeks,
      • Martino R
      • Foley N
      • Bhogal S
      • Diamant N
      • Speechley M
      • Teasell R.
      Dysphagia after stroke: incidence, diagnosis, and pulmonary complications.
      ,
      • Cohen DL
      • Roffe C
      • Beavan J
      • et al.
      Post-stroke dysphagia: a review and design considerations for future trials.
      given the severity of poststroke respiratory complications, appropriate and effective early interventions for dysphagia is crucial.
      Clinical therapy for dysphagia can be broadly divided into compensatory and remedial approaches. The compensatory approach aims to provide safer swallowing with control of food intake, material, viscosity, and the use of specific postures (eg, chin tuck, head rotation, and tilting).
      • Woo HS
      • Park SH
      • Jung MY
      • Yoo EY
      • Park JH.
      The effects of cranio-cervical flexion on activation of swallowing-related muscles.
      However, the effect of this approach is partial and temporary. This is because the patient's secretions (saliva) mixed with bacteria are much more likely to cause pneumonia or chest infections compared with food intake.
      • Hilker R
      • Poetter C
      • Findeisen N
      • et al.
      Nosocomial pneumonia after acute stroke: implications for neurological intensive care medicine.
      The close association between the aspiration of bacteria-laden secretions and the development of pneumonia has been well documented.
      • Hilker R
      • Poetter C
      • Findeisen N
      • et al.
      Nosocomial pneumonia after acute stroke: implications for neurological intensive care medicine.
      ,
      • Langmore SE
      • Terpenning MS
      • Schorck A
      • et al.
      Predictors of aspiration pneumonia: how important is dysphagia?.
      Langdon et al
      • Langdon PC
      • Lee AH
      • Binns CW.
      Dysphagia in acute ischaemic stroke: severity, recovery and relationship to stroke subtype.
      reported that of the 13 respiratory infections that were documented, 6 (46%) were observed in survivors who were ‘‘nil by mouth.” Hence, their infections were unlikely a result of aspirating food or fluids compared with their saliva secretions. Compared with compensatory-based approaches, remedial-based approaches to swallowing therapy focus on rehabilitating damaged neural and musculoskeletal structures that contribute to dysphagia through various exercises and maneuvers (eg, Mendelsohn maneuver, supraglottic swallowing, and neuromuscular electrical stimulation) in people with stroke.
      • Fujiwara S
      • Ono T
      • Minagi Y
      • et al.
      Effect of supraglottic and super-supraglottic swallows on tongue pressure production against hard palate.
      ,
      • McCullough GH
      • Kim Y.
      Effects of the Mendelsohn maneuver on extent of hyoid movement and UES opening poststroke.
      Dysphagia in people with a history of stroke is often characterized by impairments in both swallowing efficiency and safety, as well as impairments in spatial and temporal pharyngeal swallowing kinematics.
      • Martino R
      • Foley N
      • Bhogal S
      • Diamant N
      • Speechley M
      • Teasell R.
      Dysphagia after stroke: incidence, diagnosis, and pulmonary complications.
      Aspiration has been found to cause approximately 60% of poststroke pneumonia.
      • Johnston KC
      • Li JY
      • Lyden PD
      • et al.
      Medical and neurological complications of ischemic stroke: experience from the RANTTAS trial.
      Hence, the pharyngeal phase is the most important, because aspiration is most likely to occur during this phase.
      • Kidd D
      • Lawson J
      • Nesbitt R
      • MacMahon J.
      Aspiration in acute stroke: a clinical study with videofluoroscopy.
      Breathing and swallowing processes occur through similar anatomic pharyngeal structures and are controlled by the brainstem. The 2 processes must be closely coordinated because they cannot be performed simultaneously.
      • Guillén-Solà A
      • Messagi Sartor M
      • Bofill Soler N
      • Duarte E
      • Barrera MC
      • Marco E
      Respiratory muscle strength training and neuromuscular electrical stimulation in subacute dysphagic stroke patients: a randomized controlled trial.
      Also, the 2 coordinated processes provide important functions related to airway protection, such as forceful coughing. Evidence shows that reduced levels of cough flow indicate the need for assisted airway clearance and are associated with higher risk of aspiration, and therefore aspiration pneumonia in stroke.
      • Smith Hammond CA
      • Goldstein LB
      • Horner RD
      • et al.
      Predicting aspiration in patients with ischemic stroke: comparison of clinical signs and aerodynamic measures of voluntary cough.
      ,
      • Bott J
      • Blumenthal S
      • Buxton M
      • et al.
      Guidelines for the physiotherapy management of the adult, medical, spontaneously breathing patient.
      However, weakness in the respiratory muscles and lack of the required coordination secondary to central nervous lesions can lead to swallowing impairment and ineffective cough after stroke. This predisposes patients to aspiration, secretion retention, pneumonia, or even respiratory failure.
      • Martín-Valero R
      • De La Casa
      • Almeida M
      • Casuso-Holgado MJ
      • et al.
      Systematic review of inspiratory muscle training after cerebrovascular accident.
      ,
      • Finder JD
      • Birnkrant D
      • Carl J
      • et al.
      Respiratory care of the patient with Duchenne muscular dystrophy: ATS consensus statement.
      Thus respiratory (inspiratory and/or expiratory) muscle training may be a therapeutic strategy to reduce aspiration risk and prevent respiratory complications to improve swallowing function and effective cough in stroke survivors.
      To our knowledge, only 1 systematic review examined the effect of respiratory muscle training on reducing pneumonia incidence after stroke.
      • Menezes KK
      • Nascimento LR
      • Ada L
      • et al.
      Respiratory muscle training increases respiratory muscle strength and reduces respiratory complications after stroke: a systematic review.
      The likelihood of respiratory complications was observed to have reduced significantly in patients after intervention (RR, 0.38; 95% CI, 0.15-0.96; I2=0%) compared with patients who received no or sham respiratory intervention. However, the study only included 2 trials
      • Kulnik ST
      • Birring SS
      • Moxham J
      • et al.
      Does respiratory muscle training improve cough flow in acute stroke? Pilot randomized controlled trial.
      ,
      • Messaggi-Sartor M
      • Guillen-Solà A
      • Depolo M
      • et al.
      Inspiratory and expiratory muscle training in subacute stroke: a randomized clinical trial.
      (N=179 participants) and failed to further explain the reason for lower pneumonia incidence after intervention. Three systematic reviews have examined the effect of expiratory muscle training on swallowing function.
      • Mancopes R
      • Smaoui S
      • Steele CM.
      Effects of expiratory muscle strength training on videofluoroscopic measures of swallowing: a systematic review.
      • Brooks M
      • McLaughlin E
      • Shields N.
      Expiratory muscle strength training improves swallowing and respiratory outcomes in people with dysphagia: a systematic review.
      • Wang Z
      • Wang Z
      • Fang Q
      • et al.
      Effect of expiratory muscle strength training on swallowing and cough functions in patients with neurological diseases: a meta-analysis.
      The review by Renata et al
      • Mancopes R
      • Smaoui S
      • Steele CM.
      Effects of expiratory muscle strength training on videofluoroscopic measures of swallowing: a systematic review.
      failed to find clear evidence due to heterogeneity in the etiologies and differences in the methods that summarized participant performance. The review by Marinda et al
      • Brooks M
      • McLaughlin E
      • Shields N.
      Expiratory muscle strength training improves swallowing and respiratory outcomes in people with dysphagia: a systematic review.
      included 3 studies using 4 different outcome measures (Penetration-Aspiration Scale [PAS], Functional Oral Intake Scale [FOIS], surface electromyography of suprahyoid muscle activity, and hyolaryngeal movement). This study demonstrated that expiratory muscle training resulted in decreased aspiration, with a large effect for fluids and a moderate effect for solids. The meta-analysis performed by Zhuo et al
      • Wang Z
      • Wang Z
      • Fang Q
      • et al.
      Effect of expiratory muscle strength training on swallowing and cough functions in patients with neurological diseases: a meta-analysis.
      included 5 studies that reported PAS scores. They found that patients in the expiratory muscle training group had a significant reduction in PAS scores (RR, −0.94; 95% CI, −1.27 to −0.61; P<.01) compared with the control group. With regard to cough function after stroke, very few systematic reviews have examined the effect of respiratory muscle training. The meta-analysis performed by Zhuo et al
      • Wang Z
      • Wang Z
      • Fang Q
      • et al.
      Effect of expiratory muscle strength training on swallowing and cough functions in patients with neurological diseases: a meta-analysis.
      included 4 studies that analyzed cough function, with 2 outcomes (ie, peak expiratory flow rate and cough volume acceleration [CVA]). However, this meta-review failed to observe any effect on peak expiratory flow rate (RR, 0.57; 95% CI, 0.62-1.77; P=.35) or CVA (RR, 33.87; 95% CI, −57.11 to 124.85; P=.47). The systematic review by Lucy et al
      • Templeman L
      • Roberts F.
      Effectiveness of expiratory muscle strength training on expiratory strength, pulmonary function and cough in the adult population: a systematic review.
      only included 2 trials that evaluated cough function in an adult population. No significant effect of expiratory muscle training on peak expiratory cough flow of voluntary cough (PECF-VC; increased by 4.63 L/min; 95% CI, –27.48 to 36.74; P=.78) was observed. However, all the reviews mentioned above analyzed patients with dysphagia from a variety of neurological diseases or from healthy adults. Therefore, heterogeneity of the etiologies confounded their findings. Furthermore, in addition to voluntary cough function, reflex cough function should also be examined. Several studies have demonstrated that reflex cough is also associated with pneumonia risk
      • Smith Hammond CA
      • Goldstein LB
      • Horner RD
      • et al.
      Predicting aspiration in patients with ischemic stroke: comparison of clinical signs and aerodynamic measures of voluntary cough.
      ,
      • Bott J
      • Blumenthal S
      • Buxton M
      • et al.
      Guidelines for the physiotherapy management of the adult, medical, spontaneously breathing patient.
      and the function of reflex cough may be more important compared with voluntary cough in ensuring adequate airway protection and clearance after stroke.
      • Masiero S
      • Pierobon R
      • Previato C
      • et al.
      Pneumonia in stroke patients with oropharyngeal dysphagia: a six-month follow-up study.
      ,
      • Canning BJ.
      Anatomy and neurophysiology of the cough reflex: ACCP evidence-based clinical practice guidelines.
      Hence, there is a need for a more updated review of the current evidence on the effectiveness of respiratory muscle training.
      The research questions for this systematic review were: (1) Does respiratory muscle training reduce the occurrence of respiratory complications in stroke survivors; and (2) Does respiratory muscle training improve dysphagia (swallowing and cough function) after a stroke?

      Methods

      Search strategy

      All searches were conducted before August 10, 2021 using Cochrane Library, Excerpta Medical Database (EMBASE), PUBMED, and Web of Science to locate studies published in English, and using the China Biology Medicine (CBM), China Science and Technology Journal Database (VIP), China National Knowledge Infrastructure (CNKI), and Wanfang Database for studies published in Chinese. MeSH terms combined with free terms were used to search for potentially relevant articles across databases, and keywords were structured using the population, intervention approach, such as “Breathing Exercises,” “Respiratory Muscle Training,” “Maximal Respiratory Pressures,” and “Stroke.” Full search strategies are presented in appendix 1. This study conforms to all PRISMA guidelines and reports the required information accordingly. Using predetermined inclusion and exclusion criteria, 2 researchers who specialize in rehabilitation medicine independently screened each item for relevance by title and abstract. In cases where a decision could not be made as to whether the eligibility criteria were met based on the title and abstract, the full text of the article was obtained. More rigorous and comprehensive screening was used for 52 full texts by retrieving the study designs, specific interventions, characteristics of participants, and outcomes. After evaluating full-text articles, 41 studies failing to meet the inclusion criteria were excluded. Finally, 11 studies were included in this systematic review. Figure 1 outlines the flow of studies through the review. There was no potential for bias within the 2 researchers and disagreements or ambiguities were resolved by consensus with a third coauthor.

      Eligibility criteria

      The studies were included if they met the PICOS criteria as follows: (1) population (P; all of patients were adults older than 18 years diagnosed with stroke); (2) intervention (I): respiratory muscle training aimed at increasing strength of the inspiratory or expiratory muscles by using threshold resistance trainer or flow-oriented resistance trainer was considered as the intervention; (3) control (C): sham intervention without effective respiratory muscle training or no intervention was considered as the control; (4) outcomes (O): the occurrence of respiratory complications (lung infections or pneumonia) as primary outcome and swallowing function and cough function as secondary outcomes; and (5) study design (S): randomized controlled trials (RCTs). Studies were excluded if they were systematic reviews, tutorial articles, conference abstracts or single case reports; if the authors failed to obtain full texts or extract valid outcome data; if they were limited to describing immediate effects rather than outcomes after a course of treatment; if participants had swallowing dysfunction before stroke; and if, except for stroke, participants had other diseases that might affect outcomes, such as heart disease, chronic obstructive pulmonary disease, or spinal deformity.

      Quality assessment

      The Cochrane risk-of-bias criteria
      for assessing the risk of bias was used to evaluate the methodological quality of each included RCT. There are 7 items that assess bias, including random sequence generation (selection bias), allocation concealment (selection bias), blinding of participants and personnel (performance bias), blinding of outcome assessment (detection bias), incomplete outcome data (attrition bias), selective reporting (reporting bias), and other bias. Each item was categorized as low, high, or unclear risk under the guidelines stated in the Cochrane Handbook. Other bias in this review was defined as trials in which baseline characteristics were not similar between different intervention groups. A GRADE evidence profile is a specific, tabular presentation of key information about all relevant outcomes of alternative health care interventions and it was provided to present information about the body of evidence and judgments about the certainty of underlying evidence for each outcome.

      Data synthesis and analysis

      Two reviewers independently extracted data and information. Basic information such as the first author's name, publication year, study design, patient characteristics, and intervention details was extracted and analyzed. Primary outcome is the occurrence of respiratory complications that was extracted as number of participants with diagnosis of pneumonia or lung infection after commencement of training. Secondary outcomes would be represented by swallowing and cough function, such as the PAS scores, FOIS scores, PECF-VC, and peak expiratory cough flow of reflex cough (PECF-RC). The PAS is a standard tool used by both researchers and clinicians to assess penetration, aspiration, and swallowing safety
      • Steele CM
      • Grace-Martin K.
      Reflections on clinical and statistical use of the Penetration-Aspiration Scale.
      Laryngeal penetration is defined as passage of material into the larynx, which does not pass below the vocal folds, and aspiration refers to material penetrating the larynx and entering the airway below the true vocal folds. The scale is divided into 8 levels based on the depth of material penetration into the airway and whether or not the material entering the airway is expelled. Higher levels indicate a greater degree of aspiration severity. Aspiration is judged to be more severe than penetration. Therefore, aspiration is scored 6, 7, or 8. Penetration, on the other hand, is scored either 2 or 3 if residue remains above the vocal folds and 4 or 5 if residue courses to the level of the vocal folds.
      • Rosenbek JC
      • Robbins JA
      • Roecker EB
      • et al.
      A penetration-aspiration scale.
      The FOIS was developed by Crary et al
      • Crary MA
      • Mann GD
      • Groher ME.
      Initial psychometric assessment of a functional oral intake scale for dysphagia in stroke patients.
      in 2005 as a tool with very good reliability, validity, and sensitivity to objectively determine and monitor the range of oral intake of patients with neurogenic dysphagia. It is an ordinal scale with 7 tiers that assesses the oral intake of food and liquids. Different ranges of nonoral feeding are subsumed in levels 1 through 3, whereas different ranges of oral feeding are included in levels 4 through 7. Level 1 indicates complete impairment of oral intake, whereas level 7 indicates that the patient has complete oral intake regardless of food consistency or type.
      PECF was used as a surrogate marker for effective cough, which is an important defense against penetration and aspiration.
      • Fontana GA
      • Lavorini F.
      Cough motor mechanisms.
      It was measured by having the patient inspire fully and then cough forcibly through a mask or mouthpiece attached to a peak flow meter. Voluntary cough was assessed by asking participants to make repeated maximal cough efforts into a tight-fitting face mask. Involuntary coughs were usually induced by the nebulization of escalating concentrations of capsaicin through the face mask. PECF less than 160 L per minute identifies patients with an ineffective cough. Patients with PECF between 160 and 270 L per minute are at risk of respiratory tract infections, which can further decrease muscle strength.
      • Fontana GA
      • Lavorini F.
      Cough motor mechanisms.
      • Bach JR
      • Saporito LR.
      Criteria for extubation and tracheostomy tube removal for patients with ventilatory failure. A different approach to weaning.
      • Bach JR
      • Ishikawa Y
      • Kim H.
      Prevention of pulmonary morbidity for patients with Duchenne muscular dystrophy.
      • Sancho J
      • Servera E
      • Díaz J
      • Marín J.
      Comparison of peak cough flows measured by pneumotachograph and a portable peak flow meter.
      The meta-analysis was performed using Review Manager 5.3 softwarea based on the preferred reporting items of the systematic review and meta-analysis guidelines. Heterogeneity was assessed by examining the clinical characteristics of the included studies and by formal statistical testing with chi-square and I2 tests. For the assessment of swallowing function (PAS/ FOIS scores), inverse variance estimates with a fixed-effect analytical model preferred to be used to calculate the mean difference or standardized mean difference and their 95% CIs. For the occurrence of respiratory complications, the Mantel-Haenszel method with a fixed-effect analytical model preferred used to calculate relative risk (RR) and absolute risk difference and 95% CIs. If zero events were reported for one group in a comparison, a value of 0.5 was added to both groups for each such study. Based on the practice recommendation of the Cochrane Handbook,
      trials with zero events in both the intervention and control groups were not included in the meta-analysis when RRs were calculated. If there was significant between-trial heterogeneity according to the judgment before the calculation, sensitivity analysis, subgroup analysis, or meta-regression was be used to try to explain the source of heterogeneity and resolve it. On the contrary, if resolution of heterogeneity failed, a randomized-effect analytical model was applied.

      Results

      Flow of trials through the review

      The search strategy identified 2334 potentially relevant papers; 589 were found to be duplicates. After screening titles, abstracts, and reference lists, 52 potentially relevant full articles were screened. After evaluating full-text articles, 41 studies failing to meet the inclusion criteria were excluded, and 11 studies were included in this systematic review. Figure 1 outlines the flow of studies through the review.

      Characteristics of included trials

      The 11 included trials
      • Guillén-Solà A
      • Messagi Sartor M
      • Bofill Soler N
      • Duarte E
      • Barrera MC
      • Marco E
      Respiratory muscle strength training and neuromuscular electrical stimulation in subacute dysphagic stroke patients: a randomized controlled trial.
      ,
      • Kulnik ST
      • Birring SS
      • Moxham J
      • et al.
      Does respiratory muscle training improve cough flow in acute stroke? Pilot randomized controlled trial.
      ,
      • Messaggi-Sartor M
      • Guillen-Solà A
      • Depolo M
      • et al.
      Inspiratory and expiratory muscle training in subacute stroke: a randomized clinical trial.
      ,
      • Eom MJ
      • Chang MY
      • Oh DH
      • et al.
      Effects of resistance expiratory muscle strength training in elderly patients with dysphagic stroke.
      • Wang JJ
      • Zhang WW.
      A study on the feasibility of respiratory muscle training to prevent pulmonary infection after stroke.
      • Liaw MY
      • Hsu CH
      • Leong CP
      • et al.
      Respiratory muscle training in stroke patients with respiratory muscle weakness, dysphagia, and dysarthria - a prospective randomized trial.
      • Parreiras de Menezes KK
      • Nascimento LR
      • Ada L
      • et al.
      High-intensity respiratory muscle training improves strength and dyspnea poststroke: a double-blind randomized trial.
      • Moon JH
      • Jung JH
      • Won YS
      • Cho HY
      • Cho K.
      Effects of expiratory muscle strength training on swallowing function in acute stroke patients with dysphagia.
      • Park JS
      • Oh DH
      • Chang MY
      • et al.
      Effects of expiratory muscle strength training on oropharyngeal dysphagia in subacute stroke patients: a randomised controlled trial.
      • Yoo HJ
      • Pyun SB.
      Efficacy of bedside respiratory muscle training in patients with stroke: a randomized controlled trial.
      • Choi HE
      • Jo GY
      • Do HK
      • et al.
      Comprehensive respiratory muscle training improves pulmonary function and respiratory muscle strength in acute stroke patients.
      involved 523 participants and investigated the effect of respiratory muscle training on respiratory complications (n=7), swallowing function (n=5), and cough function (n=4) after stroke. Ten studies performed respiratory muscle training with a threshold resistance trainer for inspiratory or expiratory muscle. The trainer was set to various pressures ranging from 30% to 60% maximal inspiratory pressure or 15% to 75% maximal expiratory pressure). One study performed respiratory muscle training with a flow-oriented resistance trainer, the resistance of which was adjusted according to tolerance. Two of included trials
      • Kulnik ST
      • Birring SS
      • Moxham J
      • et al.
      Does respiratory muscle training improve cough flow in acute stroke? Pilot randomized controlled trial.
      ,
      • Wang JJ
      • Zhang WW.
      A study on the feasibility of respiratory muscle training to prevent pulmonary infection after stroke.
      were carried out with 3 arms of interest: inspiratory muscle training, expiratory muscle training, and sham training. For the outcomes of respiratory complications and cough function, data of each experimental subgroup were combined in different approaches to create a single comparison, following Cochrane recommendations.
      Additional relevant characteristics of the included studies and intervention are shown in tables 1 and 2.
      Table 1Characteristic of included trials
      StudyDesignInterventionOutcomeMeasurement of Rc or Cf
      Frequency and DurationParameters
      Eom et al,
      • Eom MJ
      • Chang MY
      • Oh DH
      • et al.
      Effects of resistance expiratory muscle strength training in elderly patients with dysphagic stroke.


      2017,

      Korea

      RCT

      (NR)

      N=26

      Exp (n=13): EMT

      25 reps × 5/wk × 4 wk

      Con (n=13): sham (no loading)

      25 reps × 5/wk × 4 wk
      Muscles: expiratory

      Device: EMST150

      Resistance: 70% MEP

      Progression: fixed
      Swallowing function: PAS (0-8) (by VFSS)

      Timing: 0, 4 wk
      Guillen-Solà et al,
      • Guillén-Solà A
      • Messagi Sartor M
      • Bofill Soler N
      • Duarte E
      • Barrera MC
      • Marco E
      Respiratory muscle strength training and neuromuscular electrical stimulation in subacute dysphagic stroke patients: a randomized controlled trial.


      2016,

      Spain
      RCT

      (computer-

      generated random list)

      N=33
      Exp 1 (n=16): IEMT

      50 reps × 2/d × 5/wk × 3 wk

      Con (n=17): nothing
      Muscles: inspiratory + expiratory

      Device: Orygen-dual valve

      Resistance: 30% MIP + 30% MEP

      Progression: resistance increased weekly at intervals of 10 cmH2O
      Respiratory complications:

      pneumonia

      Swallowing function:

      PAS (0-8) (by VFSS)

      FOIS (1-7)

      Timing: 0, 3, 12 wk
      Rc: chest x-ray or by fever with abnormal respiratory signs (medical reports and/or telephone interview)

      Timing: 0, 12 wk
      Wang et al,
      • Wang JJ
      • Zhang WW.
      A study on the feasibility of respiratory muscle training to prevent pulmonary infection after stroke.


      2019,

      China
      RCT

      (NR)

      N=98
      Exp 1 (n=33): EMT

      50 reps × 4/wk × 90 d

      Exp 2 (n=32): IMT

      50 reps × 4/wk × 90 d

      Con (n=33): sham (10% MIP/MEP)

      50 reps × 4/wk × 90 d
      Muscles: inspiratory or expiratory

      Device: NR

      Resistance: 50% MIP or 50% MEP

      Progression: resistance readjusted according to tolerance

      Respiratory complications: pneumonia

      Cough function:

      PECF-VC (L/min)

      PECF- RC (L/min)

      Timing: 0, 28, 90 d
      Rc: chest x-ray or by fever with abnormal respiratory signs (medical reports and/or telephone interview)

      Timing: 0, 90 d

      Cf: comprehensive lung function instrument (VIA-SYS, USA )

      VC: repeated maximal cough efforts

      RC: induced by capsaicin

      Timing: 0, 28, 90 d
      Kulnik et al,
      • Kulnik ST
      • Birring SS
      • Moxham J
      • et al.
      Does respiratory muscle training improve cough flow in acute stroke? Pilot randomized controlled trial.


      2015,

      United Kingdom
      RCT

      (random number)

      N=78
      Exp 1 (n=27): EMT

      50 reps × 7/wk × 4 wk

      Exp 2 (n=26): IMT

      50 reps × 7/wk × 4 wk

      Con (n=25): sham (10% of maximal mouth pressure)

      50 reps × 7/wk × 4 wk
      Muscles: inspiratory or expiratory

      Device: NR

      Resistance: 50% MIP or 50% MEP

      Progression: resistance adjusted to 50% of maximal strength weekly

      Respiratory complications: pneumonia

      Cough function:

      PECF-VC (L/min)

      PECF-RC (L/min)

      Timing: 0, 28, 90 d
      Rc: temperature >37.5°C on 2 consecutive measurements or a single measurement of >38.0°C with chest symptoms, and ≥1 of the following: white cell count >11000/mL, pulmonary infiltrate on chest radiograph, positive microbiology cultures

      Timing: 0, 90 d

      Cf: calibrated pneumotachograph (PK Morgan Ltd, Rainham, England)

      VC: repeated maximal cough efforts

      RC: induced by the capsaicin

      Timing: 0, 28, 90 d
      Liaw et al,
      • Liaw MY
      • Hsu CH
      • Leong CP
      • et al.
      Respiratory muscle training in stroke patients with respiratory muscle weakness, dysphagia, and dysarthria - a prospective randomized trial.


      2020,

      China (Taiwan)

      RCT

      (random number)

      N=21
      Exp (n=10): IEMT

      30 reps × 1-2/d × 5/wk × 6 wk

      Con (n=11): nothing
      Muscles: inspiratory + expiratory

      Device: Dofin breathing trainer

      Resistance: (30%-60%) MIP + (15%-75%) MEP

      Progression: resistance was adjusted according to tolerance
      Swallowing function:

      FOIS (1-7)

      Cough function:

      PECF (L/min)

      Timing: 0, 6 wk
      Cf: by a spirometer (Vitalograph, Serial Spirotrac, Buckingham, VA) per American Thoracic Society standards

      Timing: 0, 6 wk
      Parreiras de Menezes et al,
      • Parreiras de Menezes KK
      • Nascimento LR
      • Ada L
      • et al.
      High-intensity respiratory muscle training improves strength and dyspnea poststroke: a double-blind randomized trial.


      2018,

      Brazil

      RCT

      (random number)

      N=37
      Exp (n=19): IEMT

      40 min × 7/wk × 8 wk

      Con (n=18): sham (0 cmH20)

      40 mins × 7/wk × 8 wk
      Muscles: inspiratory+ expiratory

      Device: Orygen-dual valve

      Resistance: 50% MIP+ 50% MEP

      Progression: resistance adjusted to 50% maximal strength weekly
      Respiratory complications

      Timing: 0.8, 12 wk
      Rc: by asking the participants whether and how often they were admitted to a hospital due to respiratory reasons

      Timing: 0, 12 wk
      Messaggi-Sartor et al,
      • Messaggi-Sartor M
      • Guillen-Solà A
      • Depolo M
      • et al.
      Inspiratory and expiratory muscle training in subacute stroke: a randomized clinical trial.


      2015,

      Spain

      RCT

      (random number)

      N=101
      Exp (n=54): IEMT

      50 reps × 2/d × 5/wk × 3 wk

      Con (n=47): sham (10 cmH2O)

      50 reps × 2/day × 5/wk × 3 wk
      Muscles: inspiratory+ expiratory

      Device: Orygen-dual valve

      Resistance: 30% MIP+ 30% MEP

      Progression: resistance increased 10 cmH2O weekly
      Respiratory complications:

      lung infections

      Timing: 0, 3 wk, 6 mo
      Rc: chest x-ray or fever with abnormal clinical respiratory signs (medical records and telephone interviews)

      Timing: 0, 6 mo
      Moon et al,
      • Moon JH
      • Jung JH
      • Won YS
      • Cho HY
      • Cho K.
      Effects of expiratory muscle strength training on swallowing function in acute stroke patients with dysphagia.


      2017,

      Korea

      RCT

      (NR)

      N=18
      Exp (n=9): EMT

      30 min × 5/wk × 4 wk

      Con (n=9): nothing

      Muscles: expiratory

      Device: EMST150

      Resistance: 70% MEP

      Progression: fixed
      Swallowing function:

      PAS (0-8) (by VFSS)

      Timing: 0, 4 wk
      Park et al,
      • Park JS
      • Oh DH
      • Chang MY
      • et al.
      Effects of expiratory muscle strength training on oropharyngeal dysphagia in subacute stroke patients: a randomised controlled trial.


      2016,

      Korea

      RCT

      (random envelopes )

      N=27
      Exp (n=14): EMT

      25 reps × 5/wk × 4 wk

      Con (n=13): sham (no spring loading)

      Muscles: expiratory

      Device: NR

      Resistance: 70% MEP

      Progression: fixed
      Swallowing function:

      PAS (0-8)

      FOIS (1-7)

      Timing: 0, 4 wk
      Yoo et al,
      • Yoo HJ
      • Pyun SB.
      Efficacy of bedside respiratory muscle training in patients with stroke: a randomized controlled trial.


      2018,

      Korea

      RCT

      (computer-

      generated random list)

      N=40
      Exp (n=20): IMT + EMT

      30 min × 2/day × 5/wk × 3 wk

      Con (n=20): nothing

      Muscles: inspiratory+ expiratory

      Device: flow-oriented incentive spirometer +Acapella vibratory PEP device

      Resistance: not quantitative

      Progression: resistance was adjusted according to tolerance
      Respiratory complications:

      pneumonia

      Timing: 0, 3 wk
      Rc: clinical findings: new lung infiltration on imaging studies plus clinical evidence that the infiltrate was of infectious origin, which includes the new onset of fever, purulent sputum, leukocytosis, and a decline in oxygenation

      Timing: 0, 3 wk
      Choi et al,
      • Choi HE
      • Jo GY
      • Do HK
      • et al.
      Comprehensive respiratory muscle training improves pulmonary function and respiratory muscle strength in acute stroke patients.


      2021,

      South Korea
      RCT

      (NR)

      N=44
      Exp (n=22): IMT + EMT

      30 min × 5/wk × 4 wk

      Con (n=22): nothing

      Muscles: inspiratory+ expiratory

      Device: POWERbreathe (POWERbreathe International Ltd) + Threshold IMT/PEP (Philips Respironics)

      Resistance: 5-10cm H2O (POWERbreathe) + 50% MIP (Threshold IMT) + 50% MEP (Threshold PEP)

      Progression: pressure was increased by 2 cmH2O (IMT) and 1 cmH2O (EMT) as the patients became accustomed to the resistance
      Respiratory complications: pneumonia

      Cough function:

      PECF-VC (L/min)

      Timing: 0, 4 wk
      Rc: patient interviews and review of medical records for 1 y after acute stroke

      Timing: 0, 1 y

      Cf: asthma mentor peak flow meter (Respironics)

      Timing: 0, 3 wk
      Abbreviations: Cf, cough function; Con, control group; EMT, expiratory muscle training; Exp, experimental group; IEMT, inspiratory and expiratory muscle training; IMT, inspiratory muscle training; NR, not reported; Rc, respiratory complications; RC, reflex cough; reps, repetitions; VC, voluntary cough; VFSS, videofluoroscopic swallowing study.
      Table 2Characteristics of interventions
      StudyDesignParticipantsStroke Site/HemiplegiaExp (Exp 1/Exp 2)/Con, n (%)Stroke Etiology/TypeExp (Exp 1/Exp 2)/Con, n (%)
      Eom et al,
      • Eom MJ
      • Chang MY
      • Oh DH
      • et al.
      Effects of resistance expiratory muscle strength training in elderly patients with dysphagic stroke.


      2017,

      Korea

      RCT (NR)

      N=26

      Exp (n=13):

      Age: 69.2±4.1 y

      Con (n=13):

      Age: 70.2±3.6 y

      Time since stroke: <3 mo

      All participants with dysphagia
      Middle cerebral artery

      Basal ganglia

      Midbrain

      Frontal lobe

      Internal capsule

      Pons
      9/9

      0/1

      1/0

      1/1

      1/1

      1/1
      Guillen-Solà et al,
      • Guillén-Solà A
      • Messagi Sartor M
      • Bofill Soler N
      • Duarte E
      • Barrera MC
      • Marco E
      Respiratory muscle strength training and neuromuscular electrical stimulation in subacute dysphagic stroke patients: a randomized controlled trial.


      2016,

      Spain

      RCT

      (computer-

      generated random list)

      N=33
      Exp 1 (n=16):

      Age: 67.9±10.6 y

      Con (n=17):

      Age: 68.9±7.0 y

      Time since stroke: ≤1 to ≤3 wk

      All participants with dysphagia
      Right

      Left

      Bilateral/ataxia

      40%/38.1%

      55%/57.1%

      5%/4.8%

      Atherosclerosis

      Cardioembolism

      Lacunar

      Other determined etiology

      Undetermined etiology

      Missing data
      30%/28.6%

      35%/33.3%

      0%/9.5%

      0%/0%

      35%/23.8%

      0%/4.8%
      Wang et al,
      • Wang JJ
      • Zhang WW.
      A study on the feasibility of respiratory muscle training to prevent pulmonary infection after stroke.


      2019,

      China
      RCT

      (NR)

      N=98
      Exp 1 (n=33):

      Age: 66.43±13.95 y

      Exp 2 (n=32):

      Age: 62.67±14.39 y

      Con (n=33):

      Age: 64.07±10.82 y

      Time since stroke: ≤2 wk

      Dysphagia: NR
      Left

      Right

      14/17/13

      19/15/20

      Ischemic

      Hemorrhagic

      26/23/29

      7/9/4

      Kulnik et al,
      • Kulnik ST
      • Birring SS
      • Moxham J
      • et al.
      Does respiratory muscle training improve cough flow in acute stroke? Pilot randomized controlled trial.


      2015,

      United Kingdom
      RCT

      (random number)

      N=78
      Exp 1 (n=27):

      Age: 65.7±15.4 y

      Unsafe swallow: 13 (48%)

      Exp 2 (n=26):

      Age: 62.5±14.6 y

      Unsafe swallow: 10 (38%)

      Con (n=25):

      Age: 65.1±13.9 y

      Unsafe swallow: 12 (48%)

      Time since stroke: ≤0.5 mo
      Left

      Right

      Bilateral

      Cortical

      Subcortical

      Brainstem/cerebellar

      10/8/11

      17/17/14

      —/1/—

      12/10/11

      14/12/8

      1/4/6

      Ischemic

      Hemorrhagic
      22/23/24

      5/3/1
      Liaw et al,
      • Liaw MY
      • Hsu CH
      • Leong CP
      • et al.
      Respiratory muscle training in stroke patients with respiratory muscle weakness, dysphagia, and dysarthria - a prospective randomized trial.


      2020,

      China (Taiwan)
      RCT

      (random number)

      N=21
      Exp (n=10):

      Age: 66.80±11.47 y

      Swallowing disturbance: 6 (60.00%)

      Con (n=11):

      Age: 61.18±10.69 y

      Swallowing disturbance: 8 (66.67%)

      Time since stroke: 2.67±1.46 mo
      Right

      Left
      40.00%/33.33%

      60.00%/66.66%
      Hemorrhage

      Ischemic
      40.00%/66.66%

      60.00%/33.33%
      Parreiras de Menezes et al,
      • Parreiras de Menezes KK
      • Nascimento LR
      • Ada L
      • et al.
      High-intensity respiratory muscle training improves strength and dyspnea poststroke: a double-blind randomized trial.


      2018,

      Brazil
      RCT

      (random number)

      N=37
      Exp (n=19):

      Age: 60±14 y

      Con (n=18):

      Age: 67±11 y

      Time since stroke: ≤3 mo to ≤5 y

      Swallowing disorder: NR
      Right

      Left

      Unknown
      63%/32%

      32%/58%

      5%/10%
      Ischemic

      Hemorrhagic

      Unknown
      63%/79%

      16%/16%

      21%/5%
      Messaggi-Sartor et al,
      • Messaggi-Sartor M
      • Guillen-Solà A
      • Depolo M
      • et al.
      Inspiratory and expiratory muscle training in subacute stroke: a randomized clinical trial.


      2015,

      Spain
      RCT

      (random number)

      N=101
      Exp (n=54):

      Age: 65.6±11.4 y

      Dysphagia: 81.7%

      Con (n=47):

      Age: 67.6±10.9 y

      Dysphagia: 88.7%

      Time since stroke: <3 wk
      Right

      Left
      54%/59%

      46%/41%
      Cardioembolic

      Small vessel

      Undetermined

      Atherothrombotic
      20.4%/24.5%

      18.5%/18.9%

      33.5%/30.2%

      25%/18.9%
      Moon et al,
      • Moon JH
      • Jung JH
      • Won YS
      • Cho HY
      • Cho K.
      Effects of expiratory muscle strength training on swallowing function in acute stroke patients with dysphagia.


      2017,

      Korea
      RCT

      (NR)

      N=18
      Exp (n=9):

      Age: 63.0±5.8 y

      Con (n=9):

      Age: 63.1±5.2 y

      Time since stroke: ≤1 mo

      All participants with dysphagia
      Left

      Righ
      4/5

      5/4
      Ischemic

      Hemorrhagic
      6/7

      3/2
      Park et al,
      • Park JS
      • Oh DH
      • Chang MY
      • et al.
      Effects of expiratory muscle strength training on oropharyngeal dysphagia in subacute stroke patients: a randomised controlled trial.


      2016,

      Korea
      RCT

      (random envelopes)

      N=27
      Exp (n=14):

      Age: 64.3±10.7 y

      Con (n=13):

      Age: 65.8±11.3 y

      Time since stroke: ≤6 mo

      All participants with dysphagia
      Middle cerebral artery

      Basal ganglia

      Midbrain

      Frontal lobe

      Internal capsule

      Corona radiate

      Pons
      5/4

      2/1

      2/1

      2/2

      1/2

      1/1

      1/2
      Yoo et al,
      • Yoo HJ
      • Pyun SB.
      Efficacy of bedside respiratory muscle training in patients with stroke: a randomized controlled trial.


      2018,

      Korea
      RCT

      (computer-

      generated random list)

      N=40
      Exp (n=20):

      Age: 57 (34-82) y

      Aspiration: 10%

      Con (n=20):

      Age: 65 (34-86) y

      Aspiration: 10%

      Time since stroke: ≤3 mo
      Right

      Left
      11/9

      9/11
      Ischemic

      Hemorrhagic
      11/12

      9/8
      Choi et al,
      • Choi HE
      • Jo GY
      • Do HK
      • et al.
      Comprehensive respiratory muscle training improves pulmonary function and respiratory muscle strength in acute stroke patients.


      2021,

      South Korea
      RCT

      (NR)

      N=44
      Exp (n=22):

      Age: 67.6±12.4 y

      Con (n=22):

      Age: 67.2±13.3 y

      Time since stroke: ≤2 wk

      Dysphagia: NR
      Right

      Left

      Both

      None
      5/7

      15/11

      2/3

      0/1
      Ischemic

      Hemorrhagic
      16/15

      6/7
      NOTE. Outcome measures listed are only those that were analyzed in this systematic review.
      Abbreviations: Con, control group; Exp, experimental group; NR, not reported.

      Risk of bias assessment

      The outcomes of quality assessment of the studies were input into the Review Manager 5.3 software according to the quality assessment judgment criteria (Fig 2, Fig 3). The risk of bias was assessed as low, high, or unclear risk. Most of the studies had a low risk of bias for random sequence generation, allocation concealment, blinding of participants and personnel, and blinding of outcome data. All studies had a low risk of bias for incomplete outcome data, selective reporting, and other sources of bias. Seven trials were RCTs with a clear method of randomization,
      • Guillén-Solà A
      • Messagi Sartor M
      • Bofill Soler N
      • Duarte E
      • Barrera MC
      • Marco E
      Respiratory muscle strength training and neuromuscular electrical stimulation in subacute dysphagic stroke patients: a randomized controlled trial.
      ,
      • Kulnik ST
      • Birring SS
      • Moxham J
      • et al.
      Does respiratory muscle training improve cough flow in acute stroke? Pilot randomized controlled trial.
      ,
      • Messaggi-Sartor M
      • Guillen-Solà A
      • Depolo M
      • et al.
      Inspiratory and expiratory muscle training in subacute stroke: a randomized clinical trial.
      ,
      • Liaw MY
      • Hsu CH
      • Leong CP
      • et al.
      Respiratory muscle training in stroke patients with respiratory muscle weakness, dysphagia, and dysarthria - a prospective randomized trial.
      ,
      • Parreiras de Menezes KK
      • Nascimento LR
      • Ada L
      • et al.
      High-intensity respiratory muscle training improves strength and dyspnea poststroke: a double-blind randomized trial.
      ,
      • Park JS
      • Oh DH
      • Chang MY
      • et al.
      Effects of expiratory muscle strength training on oropharyngeal dysphagia in subacute stroke patients: a randomised controlled trial.
      and 4 trials were alleged RCTs but had unknown methodology and were thus defined as possible RCTs.
      • Eom MJ
      • Chang MY
      • Oh DH
      • et al.
      Effects of resistance expiratory muscle strength training in elderly patients with dysphagic stroke.
      ,
      • Wang JJ
      • Zhang WW.
      A study on the feasibility of respiratory muscle training to prevent pulmonary infection after stroke.
      ,
      • Moon JH
      • Jung JH
      • Won YS
      • Cho HY
      • Cho K.
      Effects of expiratory muscle strength training on swallowing function in acute stroke patients with dysphagia.
      ,
      • Choi HE
      • Jo GY
      • Do HK
      • et al.
      Comprehensive respiratory muscle training improves pulmonary function and respiratory muscle strength in acute stroke patients.

      Participants

      The mean age of participants ranged from 34 to 86 years across trials. The mean time after stroke ranged from 8.8 days to 24 months. The majority of trials (87%) comprised participants who were within 3 months of stroke onset at the time of admission to the trial. In total, 242 stroke participants had dysphagia confirmed by videofluoroscopic swallowing study or bedside swallowing assessment.
      • Kulnik ST
      • Birring SS
      • Moxham J
      • et al.
      Does respiratory muscle training improve cough flow in acute stroke? Pilot randomized controlled trial.
      Bedside swallowing assessment was performed by trained nursing staff, according to an algorithm and including evaluation of level of consciousness, oromotor function, and trials of water and food. Any concerns triggered review by a speech and language therapist.

      Intervention

      In all trials, the experimental intervention was respiratory muscle training delivered by a threshold resistance trainer or flow-oriented resistance trainer. The respiratory muscle training targeted the expiratory muscles,
      • Messaggi-Sartor M
      • Guillen-Solà A
      • Depolo M
      • et al.
      Inspiratory and expiratory muscle training in subacute stroke: a randomized clinical trial.
      ,
      • Eom MJ
      • Chang MY
      • Oh DH
      • et al.
      Effects of resistance expiratory muscle strength training in elderly patients with dysphagic stroke.
      ,
      • Moon JH
      • Jung JH
      • Won YS
      • Cho HY
      • Cho K.
      Effects of expiratory muscle strength training on swallowing function in acute stroke patients with dysphagia.
      ,
      • Park JS
      • Oh DH
      • Chang MY
      • et al.
      Effects of expiratory muscle strength training on oropharyngeal dysphagia in subacute stroke patients: a randomised controlled trial.
      a combination of inspiratory and expiratory muscles,
      • Guillén-Solà A
      • Messagi Sartor M
      • Bofill Soler N
      • Duarte E
      • Barrera MC
      • Marco E
      Respiratory muscle strength training and neuromuscular electrical stimulation in subacute dysphagic stroke patients: a randomized controlled trial.
      ,
      • Liaw MY
      • Hsu CH
      • Leong CP
      • et al.
      Respiratory muscle training in stroke patients with respiratory muscle weakness, dysphagia, and dysarthria - a prospective randomized trial.
      ,
      • Parreiras de Menezes KK
      • Nascimento LR
      • Ada L
      • et al.
      High-intensity respiratory muscle training improves strength and dyspnea poststroke: a double-blind randomized trial.
      ,
      • Yoo HJ
      • Pyun SB.
      Efficacy of bedside respiratory muscle training in patients with stroke: a randomized controlled trial.
      ,
      • Choi HE
      • Jo GY
      • Do HK
      • et al.
      Comprehensive respiratory muscle training improves pulmonary function and respiratory muscle strength in acute stroke patients.
      and inspiratory and expiratory muscles to separate participants.
      • Kulnik ST
      • Birring SS
      • Moxham J
      • et al.
      Does respiratory muscle training improve cough flow in acute stroke? Pilot randomized controlled trial.
      ,
      • Wang JJ
      • Zhang WW.
      A study on the feasibility of respiratory muscle training to prevent pulmonary infection after stroke.
      Participants undertook training for 30 to 40 minutes (or 25 to 50 repetitions), 4 to 14 times per week for 3 to 13 weeks. In all trials, the control intervention was noor sham respiratory intervention.
      • Kulnik ST
      • Birring SS
      • Moxham J
      • et al.
      Does respiratory muscle training improve cough flow in acute stroke? Pilot randomized controlled trial.
      ,
      • Messaggi-Sartor M
      • Guillen-Solà A
      • Depolo M
      • et al.
      Inspiratory and expiratory muscle training in subacute stroke: a randomized clinical trial.
      ,
      • Eom MJ
      • Chang MY
      • Oh DH
      • et al.
      Effects of resistance expiratory muscle strength training in elderly patients with dysphagic stroke.
      ,
      • Wang JJ
      • Zhang WW.
      A study on the feasibility of respiratory muscle training to prevent pulmonary infection after stroke.
      ,
      • Parreiras de Menezes KK
      • Nascimento LR
      • Ada L
      • et al.
      High-intensity respiratory muscle training improves strength and dyspnea poststroke: a double-blind randomized trial.
      ,
      • Park JS
      • Oh DH
      • Chang MY
      • et al.
      Effects of expiratory muscle strength training on oropharyngeal dysphagia in subacute stroke patients: a randomised controlled trial.
      Sham intervention was delivered via a threshold trainer with no resistance valve or a small resistance of the respiratory muscle strength (10% maximal inspiratory pressure/maximal expiratory pressure or 10c mH2O).

      Outcome measures

      Occurrence of respiratory complications was measured in 7 trials
      • Guillén-Solà A
      • Messagi Sartor M
      • Bofill Soler N
      • Duarte E
      • Barrera MC
      • Marco E
      Respiratory muscle strength training and neuromuscular electrical stimulation in subacute dysphagic stroke patients: a randomized controlled trial.
      ,
      • Kulnik ST
      • Birring SS
      • Moxham J
      • et al.
      Does respiratory muscle training improve cough flow in acute stroke? Pilot randomized controlled trial.
      ,
      • Messaggi-Sartor M
      • Guillen-Solà A
      • Depolo M
      • et al.
      Inspiratory and expiratory muscle training in subacute stroke: a randomized clinical trial.
      ,
      • Wang JJ
      • Zhang WW.
      A study on the feasibility of respiratory muscle training to prevent pulmonary infection after stroke.
      ,
      • Parreiras de Menezes KK
      • Nascimento LR
      • Ada L
      • et al.
      High-intensity respiratory muscle training improves strength and dyspnea poststroke: a double-blind randomized trial.
      ,
      • Yoo HJ
      • Pyun SB.
      Efficacy of bedside respiratory muscle training in patients with stroke: a randomized controlled trial.
      ,
      • Choi HE
      • Jo GY
      • Do HK
      • et al.
      Comprehensive respiratory muscle training improves pulmonary function and respiratory muscle strength in acute stroke patients.
      ; it was reported as number of participants with pneumonia in 5 trials
      • Guillén-Solà A
      • Messagi Sartor M
      • Bofill Soler N
      • Duarte E
      • Barrera MC
      • Marco E
      Respiratory muscle strength training and neuromuscular electrical stimulation in subacute dysphagic stroke patients: a randomized controlled trial.
      ,
      • Kulnik ST
      • Birring SS
      • Moxham J
      • et al.
      Does respiratory muscle training improve cough flow in acute stroke? Pilot randomized controlled trial.
      ,
      • Wang JJ
      • Zhang WW.
      A study on the feasibility of respiratory muscle training to prevent pulmonary infection after stroke.
      ,
      • Yoo HJ
      • Pyun SB.
      Efficacy of bedside respiratory muscle training in patients with stroke: a randomized controlled trial.
      ,
      • Choi HE
      • Jo GY
      • Do HK
      • et al.
      Comprehensive respiratory muscle training improves pulmonary function and respiratory muscle strength in acute stroke patients.
      and as number of participants with lung infections in 1 trial
      • Messaggi-Sartor M
      • Guillen-Solà A
      • Depolo M
      • et al.
      Inspiratory and expiratory muscle training in subacute stroke: a randomized clinical trial.
      after the commencement of training. In Menezes et al's trial,
      • Parreiras de Menezes KK
      • Nascimento LR
      • Ada L
      • et al.
      High-intensity respiratory muscle training improves strength and dyspnea poststroke: a double-blind randomized trial.
      there was no specific information about respiratory complications. Swallowing function was measured in 5 trials using the PAS (1-8 points) in 4 trials
      • Guillén-Solà A
      • Messagi Sartor M
      • Bofill Soler N
      • Duarte E
      • Barrera MC
      • Marco E
      Respiratory muscle strength training and neuromuscular electrical stimulation in subacute dysphagic stroke patients: a randomized controlled trial.
      ,
      • Eom MJ
      • Chang MY
      • Oh DH
      • et al.
      Effects of resistance expiratory muscle strength training in elderly patients with dysphagic stroke.
      ,
      • Moon JH
      • Jung JH
      • Won YS
      • Cho HY
      • Cho K.
      Effects of expiratory muscle strength training on swallowing function in acute stroke patients with dysphagia.
      ,
      • Park JS
      • Oh DH
      • Chang MY
      • et al.
      Effects of expiratory muscle strength training on oropharyngeal dysphagia in subacute stroke patients: a randomised controlled trial.
      and FOIS (1-7 points) in 3 trials.
      • Guillén-Solà A
      • Messagi Sartor M
      • Bofill Soler N
      • Duarte E
      • Barrera MC
      • Marco E
      Respiratory muscle strength training and neuromuscular electrical stimulation in subacute dysphagic stroke patients: a randomized controlled trial.
      ,
      • Liaw MY
      • Hsu CH
      • Leong CP
      • et al.
      Respiratory muscle training in stroke patients with respiratory muscle weakness, dysphagia, and dysarthria - a prospective randomized trial.
      ,
      • Park JS
      • Oh DH
      • Chang MY
      • et al.
      Effects of expiratory muscle strength training on oropharyngeal dysphagia in subacute stroke patients: a randomised controlled trial.
      Cough function was measured in 4 trials
      • Kulnik ST
      • Birring SS
      • Moxham J
      • et al.
      Does respiratory muscle training improve cough flow in acute stroke? Pilot randomized controlled trial.
      ,
      • Wang JJ
      • Zhang WW.
      A study on the feasibility of respiratory muscle training to prevent pulmonary infection after stroke.
      ,
      • Liaw MY
      • Hsu CH
      • Leong CP
      • et al.
      Respiratory muscle training in stroke patients with respiratory muscle weakness, dysphagia, and dysarthria - a prospective randomized trial.
      ,
      • Choi HE
      • Jo GY
      • Do HK
      • et al.
      Comprehensive respiratory muscle training improves pulmonary function and respiratory muscle strength in acute stroke patients.
      using PECF-VC or PECF-RC.

      Respiratory complications

      The effect of respiratory muscle training on respiratory complications was examined by pooling the data from 7 trials.
      • Guillén-Solà A
      • Messagi Sartor M
      • Bofill Soler N
      • Duarte E
      • Barrera MC
      • Marco E
      Respiratory muscle strength training and neuromuscular electrical stimulation in subacute dysphagic stroke patients: a randomized controlled trial.
      ,
      • Kulnik ST
      • Birring SS
      • Moxham J
      • et al.
      Does respiratory muscle training improve cough flow in acute stroke? Pilot randomized controlled trial.
      ,
      • Messaggi-Sartor M
      • Guillen-Solà A
      • Depolo M
      • et al.
      Inspiratory and expiratory muscle training in subacute stroke: a randomized clinical trial.
      ,
      • Wang JJ
      • Zhang WW.
      A study on the feasibility of respiratory muscle training to prevent pulmonary infection after stroke.
      ,
      • Parreiras de Menezes KK
      • Nascimento LR
      • Ada L
      • et al.
      High-intensity respiratory muscle training improves strength and dyspnea poststroke: a double-blind randomized trial.
      ,
      • Yoo HJ
      • Pyun SB.
      Efficacy of bedside respiratory muscle training in patients with stroke: a randomized controlled trial.
      ,
      • Choi HE
      • Jo GY
      • Do HK
      • et al.
      Comprehensive respiratory muscle training improves pulmonary function and respiratory muscle strength in acute stroke patients.
      With the consideration of the effect of clinical heterogeneity, the study by Parreiras de Menezes et al
      • Parreiras de Menezes KK
      • Nascimento LR
      • Ada L
      • et al.
      High-intensity respiratory muscle training improves strength and dyspnea poststroke: a double-blind randomized trial.
      was separated because of the time limitation (3 month ≤ time since stroke ≤5 year), which was completely at the chronic stage. Others were at the early stage (acute and subacute stage, ≤3 month). Therefore a total of 6 trials (n=394) were included in the meta-analysis. The likelihood of respiratory complications was significantly lower after respiratory muscle training (RR, 0.51; 95% CI, 0.28-0.93; I2=0%; P=.03) compared with no or sham respiratory intervention (fig 4). The absolute risk difference was 0.068 and the number need to treat was 14.71.
      Fig 4
      Fig 4Respiratory complications forest plot showing RR (95% CI) of respiratory complications after respiratory muscle training versus no or sham respiratory intervention (n=394).

      Swallowing function

      PAS

      The effect of respiratory muscle training on swallowing function based on PAS was examined by pooling data from 4 trials.
      • Guillén-Solà A
      • Messagi Sartor M
      • Bofill Soler N
      • Duarte E
      • Barrera MC
      • Marco E
      Respiratory muscle strength training and neuromuscular electrical stimulation in subacute dysphagic stroke patients: a randomized controlled trial.
      ,
      • Eom MJ
      • Chang MY
      • Oh DH
      • et al.
      Effects of resistance expiratory muscle strength training in elderly patients with dysphagic stroke.
      ,
      • Moon JH
      • Jung JH
      • Won YS
      • Cho HY
      • Cho K.
      Effects of expiratory muscle strength training on swallowing function in acute stroke patients with dysphagia.
      ,
      • Park JS
      • Oh DH
      • Chang MY
      • et al.
      Effects of expiratory muscle strength training on oropharyngeal dysphagia in subacute stroke patients: a randomised controlled trial.
      However, complete data extraction failed in the Guillen-Solà et al trial.
      • Guillén-Solà A
      • Messagi Sartor M
      • Bofill Soler N
      • Duarte E
      • Barrera MC
      • Marco E
      Respiratory muscle strength training and neuromuscular electrical stimulation in subacute dysphagic stroke patients: a randomized controlled trial.
      Therefore a total of 3 trials (n= 71) were included in the meta-analysis. When a fixed-effects model was applied, respiratory muscle training decreased PAS scores by 0.81 (95% CI, –1.19 to –0.43; I2=39%; P<.0001) compared with no or sham respiratory intervention (fig 5).
      Fig 5
      Fig 5PAS forest plot showing the mean difference (95% CI) of the effect of respiratory muscle training versus no or sham respiratory intervention on PAS score (n=71).

      FOIS

      The effect of respiratory muscle training on swallowing function based on FOIS was examined by pooling data from 3 trials.
      • Guillén-Solà A
      • Messagi Sartor M
      • Bofill Soler N
      • Duarte E
      • Barrera MC
      • Marco E
      Respiratory muscle strength training and neuromuscular electrical stimulation in subacute dysphagic stroke patients: a randomized controlled trial.
      ,
      • Liaw MY
      • Hsu CH
      • Leong CP
      • et al.
      Respiratory muscle training in stroke patients with respiratory muscle weakness, dysphagia, and dysarthria - a prospective randomized trial.
      ,
      • Park JS
      • Oh DH
      • Chang MY
      • et al.
      Effects of expiratory muscle strength training on oropharyngeal dysphagia in subacute stroke patients: a randomised controlled trial.
      In Guillen-Solà et al's trial,
      • Guillén-Solà A
      • Messagi Sartor M
      • Bofill Soler N
      • Duarte E
      • Barrera MC
      • Marco E
      Respiratory muscle strength training and neuromuscular electrical stimulation in subacute dysphagic stroke patients: a randomized controlled trial.
      there was no specific postintervention data and it was reported only that FOIS improved 0.76 (SD, 1.1) points after completing intervention and 1.76 (SD, 1.1) points at the 3-month follow-up. Therefore a total of 2 trials (n= 48) were included in the meta-analysis. When a random effects model was applied, there was no significant association between respiratory muscle training and the FOIS scores, which increased by 0.47 (95% CI, –0.45 to 1.39; I2=55%; P=.32) compared with no or sham respiratory intervention (fig 6).
      Fig 6
      Fig 6FOIS forest plot showing the mean difference (95% CI) of the effect of respiratory muscle training versus no or sham respiratory intervention on FOIS score (n=48).

      Cough function

      PECF-VC

      The effect of respiratory muscle training on cough function based on PECF-VC was examined by pooling data from 4 trials
      • Kulnik ST
      • Birring SS
      • Moxham J
      • et al.
      Does respiratory muscle training improve cough flow in acute stroke? Pilot randomized controlled trial.
      ,
      • Wang JJ
      • Zhang WW.
      A study on the feasibility of respiratory muscle training to prevent pulmonary infection after stroke.
      ,
      • Liaw MY
      • Hsu CH
      • Leong CP
      • et al.
      Respiratory muscle training in stroke patients with respiratory muscle weakness, dysphagia, and dysarthria - a prospective randomized trial.
      ,
      • Choi HE
      • Jo GY
      • Do HK
      • et al.
      Comprehensive respiratory muscle training improves pulmonary function and respiratory muscle strength in acute stroke patients.
      (n=226), When a fixed-effects model was applied, there was no significant association between respiratory muscle training and PECF-VC, which decreased by 18.70 L per minute (95% CI, –59.74 to 22.33; I2=19%; P=.37) compared with no or sham respiratory intervention (fig 7).
      Fig 7
      Fig 7PECF-VC forest plot showing the mean difference (95% CI) of the effect of respiratory muscle training versus no or sham respiratory intervention on PECF-VC in L per minute (n=226).

      PECF-RC

      The effect of respiratory muscle training on cough function based on PECF-RC was examined by pooling data from 2 trials
      • Kulnik ST
      • Birring SS
      • Moxham J
      • et al.
      Does respiratory muscle training improve cough flow in acute stroke? Pilot randomized controlled trial.
      ,
      • Wang JJ
      • Zhang WW.
      A study on the feasibility of respiratory muscle training to prevent pulmonary infection after stroke.
      (n = 161). When a fixed-effects model was applied, there was no significant association between respiratory muscle training and PECF-RC, which increased by 0.05 L per minute (95% CI, –40.78 to 40.87; I2=0%; P>.99) compared with no or sham respiratory intervention (fig 8).
      Fig 8
      Fig 8RC forest plot showing th mean difference (95% CI) of the effect of respiratory muscle training versus no or sham respiratory intervention on PECF-RC in L per minute (n=161).

      Discussion

      Safe swallowing can prevent foreign materials from aspirating into the airway during the swallowing process. An effective and strong voluntary cough could reduce penetration and aspiration by removing foreign materials, even after food enters the airway. Clinical interventions, such as improving swallowing or cough function, could reduce the occurrence of respiratory complications. Based on this assumption, this review set out to answer 2 questions: (1) Does respiratory muscle training reduce the occurrence of respiratory complications after stroke; and (2) Does respiratory muscle training improve the swallowing function after stroke?
      For the first question, this meta-analysis demonstrated that respiratory muscle training reduced the RR of respiratory complications immediately or 3 to 12 months after treatment initiation for the stroke participants who were at the early stage. However, we were unable to complete the meta-analysis for stroke participants who were at the chronic stage because only 1 study reported by Parreiras de Menezes et al
      • Parreiras de Menezes KK
      • Nascimento LR
      • Ada L
      • et al.
      High-intensity respiratory muscle training improves strength and dyspnea poststroke: a double-blind randomized trial.
      was included. This study reported that there was no significant between-group difference for respiratory complications. Although the power of analysis was increased by applying strict inclusion criteria, several limitations must be addressed. First, in the majority of trials, the incidence between the end of the intervention period and the final follow-up were captured, with some participants lost to follow-up, and only 1 trial
      • Kulnik ST
      • Birring SS
      • Moxham J
      • et al.
      Does respiratory muscle training improve cough flow in acute stroke? Pilot randomized controlled trial.
      reported data on the intention to treat. Second, there are several independent risk factors for poststroke pneumonia.
      • Finlayson O
      • Kapral M
      • Hall R
      • et al.
      Risk factors, inpatient care, and outcomes of pneumonia after ischemic stroke.
      ,
      • Hannawi Y
      • Hannawi B
      • Rao CP
      • et al.
      Stroke-associated pneumonia: major advances and obstacles.
      Therefore, a statistical model that adjusted for potential confounders for respiratory complications was applied in analysis to ensure precise results. Third, even though the early and chronic stages were separated in analysis, this study failed to separate the early stage into acute and subacute stroke stages among the 6 studies. It is assumed that a higher occurrence of respiratory complications manifests during the acute stage.
      • Martino R
      • Foley N
      • Bhogal S
      • Diamant N
      • Speechley M
      • Teasell R.
      Dysphagia after stroke: incidence, diagnosis, and pulmonary complications.
      Therefore, additional multicenter studies using larger patient cohorts and better methodological quality are required.
      For the second question, sufficient data were not provided to determine whether respiratory muscle training was able to improve swallowing function based on FOIS scores. Based on the liquid-type PAS scores, preliminary evidence from 3 trials
      • Eom MJ
      • Chang MY
      • Oh DH
      • et al.
      Effects of resistance expiratory muscle strength training in elderly patients with dysphagic stroke.
      ,
      • Moon JH
      • Jung JH
      • Won YS
      • Cho HY
      • Cho K.
      Effects of expiratory muscle strength training on swallowing function in acute stroke patients with dysphagia.
      ,
      • Park JS
      • Oh DH
      • Chang MY
      • et al.
      Effects of expiratory muscle strength training on oropharyngeal dysphagia in subacute stroke patients: a randomised controlled trial.
      demonstrated a reduction in the scores after respiratory muscle training. Possible explanations for this “seemingly contradictory result” could be due to several reasons. First, FOIS documents the functional level of oral intake food and liquid, as well as considering the use of enteral nutrition. Enteral nutrition may be necessary to avoid malnutrition in cases of severe dysphagia.
      • Ojo O.
      Enteral feeding tubes: not perfect but necessary.
      PAS as an objective evaluation describes fundamental aspects of dysphagia, but clinical outcome can be influenced by other important parameters (eg, awareness, collaboration, cognitive abilities, presence of apraxia, or speech impairment like aphasia), which can compromise the ability to understand language. The presence of these types of impairment can add further difficulties in the deglutition process and may reduce the success rate of swallowing treatment. Second, a previous cross-sectional study
      • Nordio S
      • Di Stadio A
      • Koch I
      • et al.
      The correlation between pharyngeal residue, penetration/aspiration and nutritional modality: a cross-sectional study in patients with neurogenic dysphagia.
      demonstrated that FOIS, compared with PAS for identifying dysphagia for liquids, had a sensitivity of 6.3% and a specificity of 94.9%. For semisolids, the sensitivity was 6.1% and specificity was 95.5%. Thus, although the sensitivity of PAS is high, the specificity is lower than FOIS. Third, the sample size was small, with only 3 trials with 71 participants included. The results only reported liquid-type PAS scores, because most of the trials only assessed the effects of the training using standard thin liquid bolus. Only the trial performed by Park et al
      • Park JS
      • Oh DH
      • Chang MY
      • et al.
      Effects of expiratory muscle strength training on oropharyngeal dysphagia in subacute stroke patients: a randomised controlled trial.
      evaluated training using semisolid bolus. After training, they found a significant difference in liquid-type PAS scores, but not for the semisolid type PAS scores (P=.03 and .32, respectively). Comparing the levels of change for both groups, significant differences were observed for only liquid-type PAS scores (P=.03) and not for semisolid type PAS scores (P=.38). Studies have shown that 62% of survivors were provided some form of modified diet or thickened fluids or were “nil by mouth” 2 days after hospital admission, which is comparable to the literature for patients with first-ever stroke.
      • Mann G
      • Hankey GJ
      • Cameron D.
      Swallowing function after stroke: prognosis and prognostic factors at 6 months.
      ,
      • Paciaroni M
      • Mazzotta G
      • Corea F
      • et al.
      Dysphagia following stroke.
      Hence, it is important that future studies assess the swallowing function of oral intake of different bolus types to identify patterns of abnormal swallowing that may reflect different underlying etiologies of dysphagia.
      However, the positive result of the liquid-type PAS scores suggested that respiratory muscle training reduced laryngeal penetration and aspiration during liquid bolus swallowing. This has potentially important implications for the management of dysphagia in stroke survivors. Similar results were observed in previous reviews
      • Brooks M
      • McLaughlin E
      • Shields N.
      Expiratory muscle strength training improves swallowing and respiratory outcomes in people with dysphagia: a systematic review.
      ,
      • Wang Z
      • Wang Z
      • Fang Q
      • et al.
      Effect of expiratory muscle strength training on swallowing and cough functions in patients with neurological diseases: a meta-analysis.
      and showed that respiratory muscle training improved muscle and neural adaptations to recover swallowing function. Expiratory muscle training promotes the activation of the suprahyoid muscles that play a major role to elevate the hyolaryngeal complex and open the upper esophageal sphincter necessary for swallowing.
      • Wheeler KM
      • Chiara T
      • Sapienza CM.
      Surface electromyographic activity of the submental muscles during swallow and expiratory pressure threshold training tasks.
      This is known to have a direct effect on decreasing aspiration and pharyngeal residues.
      • Park JS
      • Oh DH
      • Hwang NK
      • et al.
      Effects of neuromuscular electrical stimulation combined with effortful swallowing on post-stroke oropharyngeal dysphagia: a randomised controlled trial.
      Furthermore, respiratory muscle training enhances the orofacial muscles, such as the submental, palatal, lingual, velopharyngeal, and pharyngeal musculature. This is important to coordinate bolus transport during swallowing, maintenance of swallowing safety and efficiency, and functional improvements.
      • Wheeler KM
      • Chiara T
      • Sapienza CM.
      Surface electromyographic activity of the submental muscles during swallow and expiratory pressure threshold training tasks.
      Lastly, afferent stimulation of the sensory receptors of the tongue and oropharynx provided by respiratory muscle training may increase the activity of the swallowing center in the medulla oblongata of the brainstem.
      • Park JS
      • Oh DH
      • Chang MY.
      Effect of expiratory muscle strength training on swallowing-related muscle strength in community-dwelling elderly individuals: a randomized controlled trial.
      ,
      • Kim J
      • Sapienza CM.
      Implications of expiratory muscle strength training for rehabilitation of the elderly: tutorial.
      Based on a previous study,
      • Widdicombe JG
      • Addington WR
      • Fontana GA
      • et al.
      Voluntary and reflex cough and the expiration reflex; implications for aspiration after stroke.
      voluntary coughs have been closely related to aspiration in terms of airway protection mechanism during swallowing. It was found that the intensity of coughing correlated with the risk of airway aspiration. The positive outcomes of respiratory muscle training on reducing PAS scores may indicate the ability to improve cough function. However, this meta-analysis failed to provide sufficient evidence to demonstrate any effects on PECF-VC or PECF-RC after respiratory muscle training. Possible explanations could be due to several reasons. First, even though the inspiratory and expiratory muscle strength after acute stroke patients was approximately half compared with healthy age-matched controls,
      American Thoracic Society/European Respiratory Society
      ATS/ERS statement on respiratory muscle testing.
      the weakness in cough observed in stroke patients was shown to be related to reduced cortical influences that modulate cough production, rather than peripheral muscle weakness.
      American Thoracic Society/European Respiratory Society
      ATS/ERS statement on respiratory muscle testing.
      • Ward K
      • Seymour J
      • Steier J
      • et al.
      Acute ischaemic hemispheric stroke is associated with impairment of reflex in addition to voluntary cough.
      • Lanini B
      • Bianchi R
      • Romagnoli I
      • et al.
      Chest wall kinematics in patients with hemiplegia.
      In addition to respiratory muscle weakness, changes in chest wall kinematics could also be responsible for impaired cough after stroke.
      • Lanini B
      • Bianchi R
      • Romagnoli I
      • et al.
      Chest wall kinematics in patients with hemiplegia.
      Second, although an effective cough requires coordinated activation of inspiratory and expiratory muscles, PECF requires a short duration and isometric contraction of expiratory muscles to generate maximal pressure. This suggests that expiratory muscle strength is dominant in generating PECF. However, a previous meta-analysis
      • Pollock RD
      • Rafferty GF
      • Moxham J
      • Kalra L.
      Respiratory muscle strength and training in stroke and neurology: a systematic review.
      demonstrated that respiratory muscle training improves inspiratory, but not expiratory, muscle strength. This is because active inspiratory volume is a precondition for forceful expiration or cough flow. Hence, it seems reasonable that longer training is required for restoring expiratory muscle strength. Additionally, reflex cough is believed to originate primarily in the brainstem in response to food swallowing or inhalation of noxious substance. Several studies have demonstrated that reflex cough is more important than a voluntary cough in ensuring adequate airway protection and clearance after acute stroke.
      • Canning BJ.
      Anatomy and neurophysiology of the cough reflex: ACCP evidence-based clinical practice guidelines.
      ,
      • Masiero S
      • Pierobon R
      • Previato C
      • et al.
      Pneumonia in stroke patients with oropharyngeal dysphagia: a six-month follow-up study.
      However, reflex cough produced in the laboratory does not accurately replicate the response to aspirated fluids or food, which cannot be easily studied for safety reasons and patient discomfort considerations.
      • Ward K
      • Seymour J
      • Steier J
      • et al.
      Acute ischaemic hemispheric stroke is associated with impairment of reflex in addition to voluntary cough.
      In addition, it is worth noting that peak expiratory cough flow is only one aspect to reflect cough function. Because the limitation of small sample size, other equally important measures were not included in this review, such as cough expired volume or cough volume acceleration. Thus, more studies evaluating the cough function comprehensively are recommended, before drawing definitive conclusions regarding clinically worthwhile effects in the future.
      Lastly, in this meta-analysis review, one adverse event was reported in the trial conducted by Parreiras de Menezes et al.
      • Parreiras de Menezes KK
      • Nascimento LR
      • Ada L
      • et al.
      High-intensity respiratory muscle training improves strength and dyspnea poststroke: a double-blind randomized trial.
      A study participant who was in the experimental group terminated training after 2 weeks due to chest pain. The theoretical risks of elevated thoracic pressure or repeated Valsalva maneuvers performed in patients with stroke or cardiovascular comorbidities should be seriously considered during therapy.

      Study limitations

      The main limitations of this review can be deduced from the GRADE evidence profile. The small sample size was one of the most important factors leading to imprecision in this mete-analysis, especially for the outcome of PAS scores and FOIS scores as they only included 71 and 48 samples, respectively. In addition, from the total of 11 studies included in this systematic review, 6 only recruited unilateral stroke patients; 5 recruited both unilateral and bilateral stroke patients. There is no doubt that it is better to perform subgroup analysis to allow for more precise conclusions. However, the subgroup analysis was blocked in this study as we failed to obtain the original data. Also, although the power of analysis was increased by applying strict inclusion criteria, the presence of various of risk of bias for each included study such as the risk of performance bias, attrition bias, or detection bias became the other primary factors that lower the level of evidence. In view of the relative contradiction between enlarging the sample size and more rigorous studies’ screening processes, more high quality RCTs are encouraged in the future to provide a high level of GRADE evidence.

      Conclusions

      This systematic review provides evidence that respiratory muscle training is effective in reducing the risk of respiratory complications (pneumonia, lung infection). Furthermore, it improved dysphagia by reducing penetration or aspiration during swallowing liquid bolus after stroke. The results of the meta-analysis indicated that 20 to 30 minutes of respiratory muscle training 5 times per week for 4 to 5 weeks could improve swallowing function and reduce the risk of respiratory complications after stroke. However, no significant effects of respiratory muscle training on improving cough function after stroke were observed. Additional multicenter studies using larger patient cohorts are required to validate and support these findings. Furthermore, long-term follow-up studies should be performed to measure outcomes, while avoiding bias due to confounding factors such as heterogeneity of the etiologies of dysphagia.

      Supplier

      • a.
        Review Manager 5.3; Cochrane Training.

      Appendix. Supplementary materials

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