Effectiveness of pulmonary rehabilitation on exercise capacity in adult patients with lung transplantation: a systematic review and single-arm meta-analysis

Introduction

Lung transplantation (LTx) is the last option for the treatment of end-stage lung disease that is not responsive to other treatments. As a result of advances in surgical techniques, peri-operative management, and immunosuppression strategies, the survival rate after LTx has seen a significant increase, with the median survival ranging from 4 to 6 years (1). However, exercise tolerance, as assessed by the 6-minute walking test (6MWT), is only 40–60% of the normal values, and is, therefore, still limited and poses a big obstacle to recovery after LTx (2). In addition, Bourgeois et al. have confirmed that the 6-minute walking distance (6MWD) and maximum oxygen consumption (VO₂max) are important predictors of survival after LTx (3). Muscle strength, such as handgrip force (HGF) and quadriceps force (QF), are other variables that can be used as predictor of sarcopenia and other clinical and functional outcomes after LTx (4). Polastri et al. have even reported that handgrip seems to be positively related with lung function in various clinical populations (5). This implies that improving muscle strength is essential for improving exercise capacity in LTx recipients.

Pulmonary rehabilitation (PR) is a comprehensive intervention that has many benefits for patients with chronic respiratory disease (6). Schneeberger et al. showed that PR contributes to improving exercise tolerance, muscle strength, and health-related quality of life, and reducing symptoms and hospitalization in patients with chronic respiratory disease (7). Considering these benefits, PR may also be effective in patients after LTx. Previous studies have recommended PR as an optimal treatment for patients with heart (8) or kidney transplantation (9). However, because of the complexity of LTx, there is no clear consensus of whether PR is also beneficial for this group of patients.

Evidence to support the benefits of PR after LTx has been published in a few previous reviews (10-12). However, due to the variable design of the studies on this topic, no reliable meta-analysis has been conducted so far. We try to fill in this gap, and we have performed this single-arm meta-analysis to assess the efficacy of PR in LTx recipients. We present this article in accordance with the PRISMA reporting checklist (available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-568/rc) (13).

Methods

We used a comprehensive retrieval method to search in Cochrane library and the International Prospective Register of Systematic Reviews (PROSPERO) and confirmed that no similar meta-analysis had been conducted. This single-arm meta-analysis was then registered at PROSPERO (www.crd.york.ac.uk/prospero, registration No. CRD42023460247).

Search strategy

Based on the methods employed by previously published systematic reviews in the field, we formulated a strategy to search for relevant studies in the following electronic databases: MEDLINE, Embase, CINAHL, Web of Science. Besides, we set weekly automatic updates for retrieval of relevant studies from the databases until January 2024 in order to ensure that no studies were left out. Combinations of the following keywords were used for searching: (“lung transplantation” OR “organ transplantation”) AND (“pulmonary rehabilitation” OR “exercise” OR “resistance training” OR “physical therapy” OR “aerobic exercise” OR “physical fitness” OR “balance training” OR “flexibility training” OR “stretch training” OR “education”). The search was limited to keywords and terms found in titles or abstracts. Additionally, reference lists and published systematic reviews were scanned by manual searching.

Inclusion and exclusion criteria

We screened studies according to the PICOS criteria (participants, interventions, comparators, outcomes, and study type). (I) Participants—adult LTx recipients irrespective of whether they underwent single or double LTx; (II) interventions: any form of PR (e.g., exercise, nutrition, education); (III) comparisons: preintervention; (IV) outcomes: primary outcome was exercise capacity (6MWT, VO₂max) and secondary outcomes were muscle strength (handgrip strength, quadriceps strength); (V) study design: randomized controlled trials (RCTs) or quasi-experimental studies (single-group pretest-posttest design) or cohort study; (VI) language: studies published in English.

Exclusion criteria were as follows: (I) nonexperimental studies (e.g., conference abstracts or case reports, reviews, letters); (II) studies in which most of the participants required other types of surgery, in addition to LTx, such as transplantation of other organs and other heart surgery; (III) non-English studies; (IV) studies with insufficient data even after the author was contacted.

Study selection

After duplicate studies were removed, two authors (P.W. and B.G.) independently screened the titles and abstracts of the remaining studies. A third author (S.W.) solved any disagreements that arose between the two. Finally, studies were included after full-text inspection according to the inclusion and exclusion criteria.

Data extraction

Two authors (P.W. and B.G.) were responsible for collecting data on the following variables from the eligible studies: basic information (first author, year of publication, and location), participants’ characteristics (sample size, age, sex, body mass index, and original disease), interventions prescribed (exercise components, frequency of sessions, duration, and intensity), primary and secondary outcome.

Risk of bias assessment

Two authors (P.W. and B.G.) independently performed risk of bias assessment of the included studies, and the third author (S.W.) solved any disagreements that arose. The Physiotherapy Evidence (PEDro) Scale was utilized for RCTs, and the National Heart, Lung, and Blood Institute (NHLBI) assessment tool was used for quasi-experimental studies.

Statistical analysis

In this single-arm meta-analysis, for quasi-experimental trials we compared pre- and post-intervention outcomes, whereas RCTs were compared for pre- and post-intervention outcomes in the interventional group. In addition, for some included RCTs, in which participants in both experimental and control group received different types of PR, we split them as independent quasi-experimental studies.

All data extracted from eligible studies were analyzed with STATA (version 17.0) in this meta-analysis. Heterogeneity among studies was analyzed by calculating I²: values ≥50% were considered to indicate a high degree of heterogeneity between studies. A random-effects model was used for analysis when I² was ≥50% (that is, when the heterogeneity was high), and a fixed-effects model was used when the heterogeneity was low. Besides, if the heterogeneity existed, we carried out sensitivity analysis by omitting each study one at a time to evaluate the robustness of the pooled estimates. We also performed meta-regression analysis and subgroup analysis by durations of PR (duration <4 weeks, 4≤ duration <8 weeks, 8≤ duration <12 weeks and duration ≥12 weeks) and intervals between LTx and PR (interval <1 month, 1≤ interval <12 months and interval ≥12 months) to access resources of heterogeneity. Continuous data were expressed as weighted mean difference (WMD) or standard mean difference (SMD), and 95% confidence intervals (CIs) were calculated. Moreover, we acquired data from figures in the individual study reports if it was necessary. To facilitate interpretation of SMDs, we utilized cut-offs as follows: 0.2–0.5 (small effect), 0.5–0.8 (moderate effect) and >0.8 (large effect) (14). We performed Egger’s test to assess publication bias.

Results

Study characteristics

A total of 2,845 studies were obtained after the initial search. After screening, 21 studies (15-35) [12 quasi-experimental studies (15-23,33-35) and 9 RCTs (24-32)] with 1,597 participants (57.1% male) were included in the meta-analysis (Figure 1). Twenty-one included studies were from Australia (n=5), Germany (n=5), Belgium (n=2), China (n=1), USA (n=2), Norway (n=1), Israel (n=1), Austria (n=1), Turkey (n=1), Britain (n=1) and Hungary (n=1). The published year ranged from 1998 to 2024. The type of LTx performed was reported in 18 studies with 1,039 participants (15,17-26,29-35), and the majority of the patients (70.0%) underwent double lung transplantation (DLT). Besides, 1 study reported the effects of PR on single lung transplantation (SLT) and DLT separately (24), and 2 studies recruited only DLT recipients (19,34). The time interval between LT and the start of PR ranged from 4 days to 4.6 years. All participants received immunosuppressive therapy during the PR. The baseline demographic and clinical characteristics of the study participants are summarized in Table 1.

Figure 1 Flow diagram depicting the study selection protocol in this study.

Intervention characteristics

In this meta-analysis, we included 21 studies with 33 arms. The duration of PR ranged from 3 to 24 weeks. Among 9 RCTs included, participants from 7 of these RCTs accepted PR. Participants in 19 arms received endurance training (treadmill walking and stationary cycling). Participants from 18 studies received muscle strength training (lower with or without upper limb strength training) (see Table 1).

Risk of bias assessment

The PEDro scale was used to perform risk of bias assessment for RCTs (24-32). The total score ranged from 5 to 8 (see Table 2). As a result of variations in the study design, all the participants and researchers were not blinded to the study. The results of risk of bias assessment for quasi-experimental studies are detailed in Table 3 (15-23,33-35). All the included studies clearly stated the study question, listed pre-specified inclusion criteria, comprised participants who were representative of LTx recipients, and clearly defined the intervention and outcome variables. A noteworthy observation was that the percentage of participants who were lost to follow-up was low in all the included studies; this indicates good compliance with the PR regimen.

Effects of PR on exercise capacity

Of the selected studies, 18 studies (15,16,18-22,24-26,28-35) with 33 arms (1,305 participants) reported 6MWD at the baseline and after PR. The mean 6MWD at the baseline in the participants undergoing exercise training in 14 studies was 339.6 m (range, 149.4–540.4 m), as one reported the percentage of 6MWD (31). Pooled analysis of these 18 studies revealed a significant degree of heterogeneity (I²=85.5%, P<0.001). Based on the heterogeneity results, random-effects analysis was performed, and it showed that PR had a strong correlation with improvement in 6MWD (SMD =1.28, 95% CI: 1.05–1.50, P<0.001) (Figure 2). Besides, the observed pooled effect size remained consistent according to the sensitivity analyses (Figure 3). Meta-regression analysis showed that both durations of PR (P<0.001) and intervals between LTx and PR (P<0.001) were responsible for the heterogeneity.

Figure 2 Effects of pulmonary rehabilitation on 6-minute walking distance in lung transplantation recipients. CI, confidence interval; DL, DerSimonian-Laird.

Figure 3 Sensitivity analyses of primary meta-analysis. Every effect size was located between 1.05 and 1.50 while none of 95% CI crossed the invalid line “0”, signifying that the result was stable. CI, confidence interval.

Then, we conducted subgroup analyses based on intervention duration (subgroup 1: duration <4 weeks, subgroup 2: 4≤ duration <8 weeks, subgroup 3: 8≤ duration <12 weeks and subgroup 4: duration ≥12 weeks), interval between LTx and PR (subgroup 1: interval <1 month, subgroup 2: 1≤ interval <12 months and subgroup 3: interval ≥12 months). The results of the former subgroup analyses showed a larger positive effect on 6MWD in subgroup 2 (SMD =1.46, 95% CI: 1.14–1.79, P<0.001), subgroup 3 (SMD =1.12, 95% CI: 0.67–1.57, P<0.001) and subgroup 4 (SMD =1.30, 95% CI: 0.87–1.73, P<0.001), while subgroup 1 presented small effect (SMD =0.53, 95% CI: 0.24–0.82, P=0.002) (Figure 4). In terms of heterogeneity, both subgroup 1 and 3 showed a considerable level of homogeneity (subgroup 1: I²=0.0%, P=0.46; subgroup 3: I²=0.0%, P=0.50), and between-studies heterogeneity in subgroup 4 also decreased to some extend (subgroup 4: I²=65.2%, P=0.002), whereas, subgroup 2 showed a considerable level of heterogeneity (subgroup 2: I²=91.6%, P<0.001). Besides, the latter subgroup analyses revealed that there was greater positive effect on 6MWD in subgroup 1 (SMD =1.71, 95% CI: 1.38–2.03, P<0.001) and subgroup 2 (SMD =0.93, 95% CI: 0.74–1.11, P<0.001), and small effect in subgroup 3 (SMD =0.38, 95% CI: 0.06–0.70, P=0.02) (Figure 5). The between-studies heterogeneity in three subgroups showed varying degrees of decrease (subgroup 1: I²=80.9%, P<0.001; subgroup 2: I²=56.6%, P=0.01; subgroup 3: I²=0.0%, P=0.93).

Figure 4 Subgroup analysis on the outcome of 6-minute walking distance categorized by duration of pulmonary rehabilitation [(I) duration <4 weeks; (II) 4≤ duration <8 weeks; (III) 8≤ duration <12 weeks; (IV) duration ≥12 weeks]. CI, confidence interval; DL, DerSimonian-Laird.

Figure 5 Subgroup analysis on the outcome of 6-minute walking distance categorized by interval between lung transplantation and pulmonary rehabilitation [(I) duration <1 month; (II) 1≤ duration <12 months; (III) duration ≥12 months]. CI, confidence interval; DL, DerSimonian-Laird.

Four studies (23,27,31,32) with 5 arms (110 participants) reported VO₂max at the baseline and after PR. The pooled analysis of these 4 studies showed that PR may had small effect on VO₂max in adult LTx recipients (SMD =0.42, 95% CI: 0.15–0.68, P=0.002) (Figure 6). There was no significant between-studies heterogeneity (I²=0.0%, P=0.85).

Figure 6 Effect of pulmonary on maximum oxygen consumption in lung transplantation recipients. CI, confidence interval; IV, inverse variance.

In addition to the studies mentioned above, we still included 1 study (17 participants) which evaluated the effect of PR on exercise capacity by incremental shuttle walk test (ISWT) (17), and the result also showed a positive effect. We did not perform pooled analyses because of the small number of studies.

Effects of PR on muscle strength

The effect of PR on HGF was assessed in detail in 6 studies with 7 arms (148 participants) (16,17,22,24,27,31), which showed good homogeneity (I²=0.0%, P=0.86). Based on the homogeneity, pooled fixed-effects analysis was conducted on the 6 studies, and the results demonstrated a small effect in handgrip (SMD =0.49, 95% CI: 0.26–0.73, P<0.001) (Figure 7).

Figure 7 Effect of pulmonary on hand grip force in lung transplantation recipients. CI, confidence interval; IV, inverse variance.

Seven studies with 10 arms (238 participants) reported the effect of PR on QF (17,22,27,29-31,34), which showed good homogeneity (I²=0.0%, P=0.88). Based on the homogeneity, pooled fixed-effects analysis was conducted on the 7 studies, and the results demonstrated a moderate effect in QF (SMD =0.63, 95% CI: 0.45–0.82, P<0.001) (Figure 8).

Figure 8 Effect of pulmonary on quadriceps force in lung transplantation recipients. CI, confidence interval; IV, inverse variance.

Publication bias

In terms of publication bias, the Egger’s test did not show any significant publication bias in 6MWD (P=0.14), VO₂max (P=0.50), QF (P=0.76) and HGF (P=0.38).

Discussion

The principal finding of this single-arm meta-analysis is that PR is closely related with a significant improvement in exercise capacity (based on improvements in 6MWD, VO₂max) and muscle strength (based on HGF, QF) from baseline to follow-up in LTx recipients. Although more than half of included studies were quasi-experimental design, the greatest between-studies heterogeneity may be associated with the difference in duration of PR and interval between LTx and PR. This meta-analysis makes an important contribution to the literature on this topic and has strong clinical implications, as the findings show that there is evidence of the efficacy of PR in LTx recipients and highlight its potential role as an adjunct to clinical approaches designed to improve survival.

6MWD and VO₂max are the main indicators of exercise capacity, which showed significant improvements with PR. Previous study has established an association between 6MWD and survival in patients after LTx (36). Moreover, improvement in physical capacity is known to have a positive correlation with better prognosis (36,37). As a result, improvement in 6MWD and VO₂max has been used as a surrogate endpoint in LTx clinical trials. However, most of the included studies that assessed exercise capacity were quasi-experimental studies, so it is difficult to draw a definitive conclusion on whether PR can induce a clinically viable increase in exercise capacity that can be distinguished from natural recovery. More notably, subgroup analyses on 6MWD seemed to suggest that the earlier LTx recipients undertake adequate PR, the better the exercise capacity will be. In the future, more studies are needed to confirm the effect of PR on exercise capacity in LTx recipients.

Our study also reported an improvement in HGF and QF, which is consistent with the findings of a previous study (5). Delayed recovery of exercise capacity is related to the slow recovery of muscle (38), and LTx recipients who do not receive PR are expected to experience a reduction in muscle strength due to peripheral myopathy caused by long-term drug treatment (39). Despite these optimistic findings, the clinical relevance needs to be confirmed through high-quality RCTs in the future.

LTx recipients exhibit deficiencies in muscle mitochondrial function and peripheral circulatory factors as a result of deconditioning and the impact of immunosuppressive therapy (40). Although the mechanisms underlying improvement in exercise capacity with PR among patients after LTx are not well understood. The benefits of PR are likely associated with improving these deficiencies. With regard to the influential factors, peripheral muscle abnormalities have been shown to be the predominant limiting factor to exercise capacity in LTx recipients; in addition, the original lung disease and pathophysiology may also influence an individual’s exercise capacity and physical activity (39). Recent studies have shown that exercise contributes to significant improvements in central pulmonary perfusion and peripheral skeletal muscle function that are beneficial for improvement in exercise capacity. This is probably because improved pulmonary perfusion is likely to lead to improved oxygenation and cardiac output and, thus, improvement in exercise tolerance and cardiorespiratory fitness. Moreover, Memme et al. (41) reported that exercise could help adjust the volume, structure, and capacity of mitochondria; thus, PR may help alleviate the muscle atrophy and damage to the respiratory function of mitochondria resulting from long-term immobilization before and after LTx and the use of immunosuppressive drugs. To summarize, the mechanisms underlying the beneficial effects of PR may include improvement in pulmonary effusion, peripheral skeletal muscle function, and mitochondrial structure and function. In the future, these mechanisms need to be investigated in detail in order to gain a better understanding of the effects and treatment targets.

Study limitations

There are several limitations in this study which should be noted. First, we only included studies that were published in English, which may cause language bias. Besides, we cannot eliminate a selection bias because the studies included were only retrieved from published trials. Second, significant heterogeneity may be associated with original disease, simple size, the features of the PR regimen (such as frequency, intensity, and duration of exercise), type of LTx. Although the results of this meta-analysis suggested that different PR durations and different intervals between LTx and PR may have distinct effects on 6MWD in LTx recipients, in the future, if necessary, network meta-analysis is still needed to explore for more optimized PR programs.

Conclusions

The current evidence from the literature indicates that PR is associated with significant improvement in exercise capacity among adult patients with LTx. Future high-quality studies are needed to determine whether exercise training can safely and effectively improve long-term clinical outcomes among these patients in the real-world setting.

Acknowledgments

We thank the staff of the Department of Rehabilitation Medicine and Department of Lung Transplantation in China-Japan Friendship Hospital for their assistance.

Funding: This work was supported by the Chinese Academy of Medical Sciences (CAMS) Innovation Fund for Medical Sciences (2021-12M-1-049 to W.C.) and China’s National Key R&D Programmes (2022YFC2009700 to S.J.). The funding body had no role in the design of the study or collection, analysis, or interpretation of data, nor in writing the manuscript.

Footnote

Reporting Checklist: The authors have completed the PRISMA reporting checklist. Available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-568/rc

Peer Review File: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-568/prf

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-568/coif). S.J. reports funding from the China’s National Key R&D Programmes (2022YFC2009700). W.C. reports funding from the Chinese Academy of Medical Sciences (CAMS) Innovation Fund for Medical Sciences (2021-12M-1-049). The other authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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