Key words : Lung transplantation, Physiotherapy, Respiratory muscles

Introduction

Respiratory muscle training strengthens respiratory muscles, whether inspiratory, expiratory, or both. As with all other skeletal muscles, when respiratory muscles are trained against resistance, there is an increase in strength and endurance.¹ In patients with hyperinflation in particular, a mechanical disadvan-tage of muscles leads to a gradual loss of respiratory muscle strength and ventilatory reserve over time.^1,2 In severe hyperinflation, the primary mechanism of mechanical disadvantage is the Hoover sign (paradoxical inspiratory indrawing of the lateral rib margin), with the contraction of the flattened diaphragm being insufficient to inflate the lungs.³ Loss of respiratory muscle strength and fatigue correlate with greater dyspnea in patients with chronic obstructive pulmonary disease (COPD).⁴ Moreover, studies evaluating respiratory muscle training have described positive effects on dyspnea, physical capacity, and quality of life after respiratory muscle training.^1,5 The American Thoracic Society and European Respiratory Society Pulmonary Rehabilita-tion guidelines state that respiratory muscle training can provide additional benefits in patients with respiratory muscle weakness.^6,7

Notably, expiratory airflow, particularly in obstructive disease, is largely effort-independent because of the Starling resistor nature of airflow in all but the early phase of exhalation.⁸ Expiratory muscle training strengthens expiratory muscles, which play a crucial role in forced expiration, coughing, and swallowing; indeed, it is a therapeutic option for treatment of swallowing impairments and dysphagia in patients with acute stroke and COPD and to prevent aspiration of material into the airway.^9-11 It is well known that tracheostomy, long intubation duration, and venovenous perioperative extracor-poreal membrane oxygenation are risk factors for development of postoperative aspiration after lung transplant (LT).¹² Therefore, there is room for imple-menting expiratory muscle training in LT recipients.

Nevertheless, in the literature, respiratory muscle training is predominantly reported as inspiratory muscle training (IMT).¹ Indeed, IMT is used in reha-bilitation to exercise respiratory muscles under various pathological conditions and clinical contexts.^13-25 Inspiratory muscle weakness, the increased metabolic cost of breathing, and the exacerbation of symptoms in respiratory diseases generate a vicious circle,²⁶ and IMT can be used as a therapeutic tool.^1,6,7,27 Inspiratory muscle training can be perfor-med using 2 types of trainers, resistive and threshold devices; in the first case, the resistance varies in relation to the inspiratory flow rate, whereas, in the second, it is fixed at a given value.^28-32 Volume and inspiratory flow responses to IMT with a resistive trainer have been suggested to be larger than responses with a threshold device, and resistive training allows higher loads than pressure threshold loading.³⁰

Although IMT is increasingly used in LT candi-dates and recipients, information from the literature is controversial. Here, we reviewed and summarized the literature about IMT in LT candidates and recipients and considered the associations between IMT and respiratory muscle strength, functional performance, quality of life, and lung function.

Materials and Methods

Study design
We conducted this integrative review³³ by searching 5 primary databases: the US National Library of Medicine PubMed system, Scopus, Web of Science, Cochrane Library, and Cumulative Index to Nursing and Allied Health Literature (ie, CINAHL). We used the Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines to design this review.³⁴

Search strategy
We searched databases from their inception to April 2024. Two keyword entries, “lung transplantation” and “inspiratory muscle training,” were matched using the Boolean operator AND. In each database, the following fields were searched: PubMed (all fields); Scopus (title, abstract, keywords); Web of Science (all fields); Cochrane Library (title, abstract, keywords); and CINAHL (all text). No filters were applied for document type, age, sex, publication date, and subject. We completed the search process in April 2024.

Inclusion and exclusion criteria
To be included, citations were required to be published in English and to describe IMT in patients waiting for or after receiving LT. The following types of research were considered eligible: randomized controlled trials, observational studies, research letters, and case reports. All citations that lacked a description of IMT in patients waiting for or receiving LT and/or were published in languages other than English were not eligible for inclusion. Abstracts, conference proceedings, editorials, letters to editor, and study protocols were also unsuitable for inclusion.

Selection process
We removed duplicates from the retrieved citations and screened the remaining documents for eligibility according to the abstract content. For articles with abstracts that met the inclusion criteria, we screened the full text for suitability; once confirmed, citations were considered eligible for the final analysis. Two independent reviewers who evaluated and agreed on the results assessed the studies gathered from the literature.

Results

The search process identified 119 citations. Further analysis of the references in the retrieved articles did not return additional material to be included in the present study. After duplicates were removed, 9 documents were screened for eligibility, and 7 were included in the final analysis (Figure 1). Three of 7 studies involved LT recipients,^35-37 and 4 were conducted among LT candidates.^38-41 One study was observational,³⁷ 2 were interventional,^35,38 1 was a randomized controlled trial,⁴¹ and 3 were single case studies,^36,39,40 with 1 study involving a pediatric patient.³⁶ The present review included 64 patients (47% female); 23 (36%) were LT recipients, and 41 (64%) were LT candidates. Among LT recipients, 11 (48%) were heart-lung transplant (HLT) recipients, 7 (30%) were single LT recipients, and 5 (22%) were double LT recipients (Table 1). In 6 of 7 studies, the same IMT trainer device (POWER breathe, POWERbreathe International Ltd) was used.^35,36,38-41

Although LT recipients had greater significant improvements in functional performance than LT candidates ((Table 2), (Table 3)), studies returned heterog-eneous results. For example, in 1 study, LT candidates showed no improvement in 6-minute walking distance (6-MWD) after treatmel,³⁸ However, in another trial, LT candidates improved 6-MWD by >70 m after treatment.⁴¹ Such changes were substa minimal clinically important difference for the 6-minute walking test in patients with respiratory diseases is estimated at 14 to 30.5 m.^42,43

In addition, the 11 HLT recipients showed impro-ved functional capacity, performing better at the 6-minute walking test after treatment than LT candi-dates and recipients ((Table 2), (Table 3)). Conversely, differences in maximal inspiratory pressure (MIP) before and after IMT were comparable between LT candidates and LT recipients ((Table 2), Table 3).

Inspiratory muscle training-associated effects in lung transplant recipients
The highest value of inspiratory muscle strength was observed in a series of LT recipients who, after 4 months of IMT, improved MIP by 31.8 ± 14.6 cmH₂O versus baseline (104.2 ± 14.5 cmH₂O).³⁵ In LT recipients, IMT was conducted in the context of comprehensive interventions, including physical exercise; all participants among LT recipients used a threshold trainer (Figure 2) ranging from 15% to 60% of MIP and mostly exercised twice daily for 10 to 15 minutes per session. Among LT recipients was a 13-year-old boy whose MIP increased by 63.5% after IMT (Table 1). Lung transplant recipients obtained encouraging results in other domains besides respiratory muscle strength. Indeed, studies showed that lung function and functional performance improved in individuals who participated in IMT (Table 2). The 6-MWD significantly increased in 2 studies,^35,37 and improvements were also detected in forced expiratory volume in 6 seconds, forced vital capacity,^36,37 and exercise tolerance.³⁷

Inspiratory muscle training-associated effects in lung transplant candidates
The highest inspiratory muscle strength value in the publications that we reviewed was described in an LT candidate with idiopathic pulmonary fibrosis who had exercised for 2 years with IMT, reaching MIP of 180 cmH₂O.⁴⁰ Among LT candidates, partici-pants used a threshold trainer ranging from 30% to >50% of MIP, and all participants exercised twice daily, performing 30 to 60 inspirations or for 15 minutes (Table 1).

In LT candidates who performed IMT, variations of clinical variables of rehabilitative interest were observed (Table 3). The 6-MWD increased in 2 studies,^38,41 forced expiratory volume in 1 second and forced vital capacity deteriorated over time in 2 studies,^38,40 and these factors showed improvements in another study.⁴¹ The changes were compatible with the different underlying diseases, with patients with COPD³⁸ deteriorating more than those with bronchiectasis.⁴¹

Dyspnea intensity, measured with the London Chest Activity of Daily Living scale (with higher scores indicating worse dyspnea),⁴⁴ decreased after treatment, and results were consolidated at 3-month follow-up in 1 study³⁸ (Table 3).

Quality of life also improved in a study after treatment, which showed decrease in the Saint George Respiratory Questionnaire total score, although differences were not consistent³⁸ (Table 3).

Discussion

Inspiratory muscle training is a component of the rehabilitation for LT candidates and recipients and can be performed in a home-based care setting before or after LT. The present review found that IMT-associated effects are more noticeable in domains of rehabilitative interest, such as dyspnea, quality of life, lung function, and functional performance. At the same time, IMT is an easy-to-perform technique that adults and children can perform with a simple hands-on device. In children, supervision could be necessary to ensure that the exercise is performed properly.³⁶ In this regard, it should be highlighted that, for adults, IMT can be performed with pressure-threshold loading or flow-resistive loading.⁴⁵ In a previously published review that investigated the effects of IMT in children, IMT seemed to improve breathing mechanics, reducing dyspnea; the same study provided details of type, frequency, and intensity of training, which can be used as a reference for further insights.⁴⁵

In the present review, the improvements in MIP gained by the only LT pediatric recipient were obtained by exercising with a threshold device without other forms of exercise (ie, motor activities), raising the question of whether IMT alone can improve respiratory muscle strength.³⁶ To the same extent, 22 LT candidates who exercised exclusively with IMT obtained improvements in different domains such as dyspnea, lung function, and functional performance.³⁸

Although respiratory muscle performance is correlated with dyspnea,¹⁸ only 1 of 7 studies inves-tigated dyspnea³⁸ (Table 3). This aspect stimulates further reflections because dyspnea is a prevalent symptom among patients with fibrotic deformities of the lung tissue.^46-48 Why does the current research not investigate dyspnea among patients undergoing IMT awaiting or receiving LT? This question should be addressed with further studies and stimulate additional clinical experiments.

Another matter of reflection is that, in the literature, there are published experiences describing clinical improvements in LT candidates and reci-pients in domains of rehabilitative interest in patients not subjected to IMT. Moreover, some confounders may occur after transplant; the phrenic nerve can be stunned, and steroids can worsen muscle strength.⁴⁹

Improvements in exercise capacity, lung function, dyspnea intensity, respiratory muscle strength, and quality of life have been observed in LT recipients who have attended pulmonary rehabilitation programs without IMT.^50,51 Patients in 1 study participated in an 8-week outpatient postoperative rehabilitation prog-ram 3 times per week, which included aerobic and resistance exercises,⁵⁰ whereas, in another study, patients had treatment that consisted of 40-minute in-hospital daily sessions of active range-of-motion and breathing exercises that continued at home up to 3 months once patients were discharged.⁵¹

The results of those experiences give room to the assumption that motor exercise is correlated with increased respiratory muscle strength independently by the execution of IMT. On the other hand, such a hypothesis has been also confirmed in different patient populations where respiratory muscle strength had improved without the use of IMT versus patients who performed it.⁵²

Further directions
Rehabilitation for LT candidates and recipients is continuously developing; further directions are the prediction of outcomes and treatment optimization.⁵³ In moving toward these directions, IMT could play a role in preserving and ameliorating inspiratory muscle function-related variables, such as dyspnea, functional performance, respiratory muscle strength, and lung function.

Another area worthy of further investigation is expiratory muscle strength training in LT recipients to prevent and treat postoperative swallowing impairments and aspiration phenomena.

Limitations
The present study is not without limitations; the small number of citations retrieved and the exiguity of the population are a matter of concern. On the other hand, LT is a treatment that continues to be limited by organ availability; therefore, it is not unusual that the number of studies in such a field are small. Because of the heterogeneity of the sample and different treatment intensities, some risk for immortal time bias and survivorship bias seems probable for this review.

In addition, patient age ranged from children to adult, which limited the granularity of the conclu-sions regarding specific age and diagnosis-related differential benefits. Furthermore, multiple factors other than IMT may have enhanced inspiratory muscle function. Indeed, after successful operations, the postoperative timeframe is often characterized by improved oxygenation and the restoration of the diaphragm and intercostal muscle function⁵⁴ since patients are less prone to fatigue and free from dyspnea as, for example, particularly evident in patients undergoing lung retransplant.⁵⁵ In addition, IMT was eventually associated with other rehabi-litative interventions in most of the included studies; thus, isolating the IMT effects on LT candidates and recipients was impossible.

Despite the limitations, the present review provi-des an overview of the current knowledge and represents a starting point for further analyses. Indeed, because of the ease of execution and the possibility of performing IMT at home and autono-mously, interest should not be tempered by the small number of patients reported here.

Conclusions

The present review showed that IMT can be performed by both LT candidates and recipients, in both adult and pediatric patients, and can substantially increase the inspiratory muscle strength. The magnitude of other IMT-related effects is heterogeneous and should be confirmed by further investigation.

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