key: cord-0980126-y91ozdbt
authors: Wen, Jing; Milne, Stephen; Sin, Don D.
title: Pulmonary rehabilitation in a postcoronavirus disease 2019 world: feasibility, challenges, and solutions
date: 2021-10-21
journal: Curr Opin Pulm Med
DOI: 10.1097/mcp.0000000000000832
sha: 79dcc98c89c3664c80567969d8eacf4cac296fee
doc_id: 980126
cord_uid: y91ozdbt

Pulmonary rehabilitation improves clinical outcomes in patients with chronic obstructive pulmonary disease (COPD). Traditional centre-based (in-person) pulmonary rehabilitation was largely shut down in response to the COVID-19 pandemic, forcing many centres to rapidly shift to remote home-based programs in the form of telerehabilitation (tele-pulmonary rehabilitation). This review summarizes the recent evidence for the feasibility and effectiveness of remote pulmonary rehabilitation programs, and their implications for the delivery of pulmonary rehabilitation in a postpandemic world. RECENT FINDINGS: A number of innovative adaptations to pulmonary rehabilitation in response to COVID-19 have been reported, and the evidence supports tele-pulmonary rehabilitation as a viable alternative to traditional centre-based pulmonary rehabilitation. However, these studies also highlight the challenges that must be surmounted in order to see its widespread adoption. SUMMARY: There are outstanding questions regarding the optimal model for tele-pulmonary rehabilitation. In the post-COVID-19 world, a ‘hybrid’ model may be more desirable, with some components held in person and others via telehealth technology. This would be determined by the infrastructure and expertise of individual centres, and the needs of their patients. In order to achieve a truly patient-centred pulmonary rehabilitation program, high-quality studies addressing these outstanding questions, as well as multidisciplinary collaboration, are required.

Chronic obstructive pulmonary disease (COPD) is a leading cause of morbidity and mortality worldwide [1] . Pulmonary rehabilitation is a cornerstone in the management and treatment of patients with COPD. There is robust evidence supporting the effectiveness of pulmonary rehabilitation programs in the realworld by reducing dyspnoea, improving patients' health-related quality of life (HRQoL) and exercise capacity, and enhancing their social life [2] .

Over the past 18 months, the world has been consumed by the novel coronavirus disease (COVID- 19) pandemic. Despite global efforts to control the pandemic and the implementation of mass vaccinations, infection rates remain high and healthcare systems remain under enormous pressure in many areas of the world. Patients with COPD are highly vulnerable to poor outcomes from COVID-19 [3 & ]. Accordingly, special attention has been paid to protecting COPD patients from contracting the virus through masking, physical distancing and vaccinations. These measures extend to the healthcare setting, including institutions providing pulmonary rehabilitation [4] . As pulmonary rehabilitation programs have been traditionally conducted in-person, these protective modifications necessary to reduce the spread of SARS-CoV-2 have posed enormous challenges for pulmonary rehabilitation practitioners and patients. Nevertheless, some centres have successfully adapted their programs to the new pandemic realities through the implementation of virtual care.

Here, we describe the current state of pulmonary rehabilitation programs for COPD patients during the COVID-19 pandemic, and highlight some of the challenges and potential solutions for delivering effective pulmonary rehabilitation in the postpandemic world.

This review is based on peer-reviewed articles in PubMed including randomized controlled trials (RCT), feasibility studies, pilot studies, reviews, and meta-analyses focusing on pulmonary rehabilitation that were published between January 2020 and August 2021. Some important clinical studies on this topic are summarized in Table 1 .

Pulmonary rehabilitation can be defined as a comprehensive, multidisciplinary approach to managing patients with chronic respiratory diseases (CRDs), which according to the official American Thoracic Society/European Respiratory Society (ATS/ERS) statement, is 'designed to improve the physical and psychological condition of people with CRD and to promote the long-term adherence to health-enhancing behaviors' [5] .

Although the setting and delivery of pulmonary rehabilitation vary across centres, most effective pulmonary rehabilitation (PR) programs contain five core elements: prerehabilitation assessment, supervised exercise training, body composition interventions, self-management education, and psychological and social support. These components can be delivered at an individual patient level or more commonly in a group setting approximately two to three times a week for 6-8 weeks or even longer [5, 6] . The clear benefits of pulmonary rehabilitation for COPD patients have been demonstrated in multiple RCTs, meta-analyses, and ''real-life'' observational studies. Positive impacts have been reported for endpoints, such as functional capacity [7] , muscle endurance and strength [8] , cardiorespiratory fitness [9] , breathlessness and hospital readmissions [10] . Although most of the large clinical studies have focused on COPD patients, individuals with other CRDs including those with interstitial lung disease [11] , asthma [12] , and pulmonary hypertension [13] have also benefited from PR.

Although pulmonary rehabilitation programs are heterogeneous in terms of their content and format, prior to the COVID-19 pandemic, the majority were hospital-based with multiple in-person visits. According to a global survey of pulmonary rehabilitation programs across 430 centres from 40 countries, less than 5% of pulmonary rehabilitation centres offered a home-based component and even fewer offered a standalone home-based program prior to the pandemic [14] . Most of these were maintenance extensions of initial hospitalbased pulmonary rehabilitation in the form of tele-pulmonary rehabilitation, which utilizes communication and information technologies to provide rehabilitation [15] . A systematic review of home-based pulmonary rehabilitation for CRD found that tele-pulmonary rehabilitation -either as a primary or maintenance therapy -led to similar improvements in exercise capacity, HRQoL and dyspnoea scores compared with an in-person model [16] . Additionally, tele-pulmonary rehabilitation showed an overall higher completion rate (93%) compared with that of inperson rehabilitation (70%). Importantly, no harmful effects were noted with tele-pulmonary rehabilitation. Barriers to effective pulmonary rehabilitation existed  prior to the COVID-19 pandemic, and have been  exacerbated by the pandemic because of pressures on  healthcare systems, widespread lockdowns, and the  need for social distancing. Remote pulmonary rehabilitation delivered using telecommunications and other technologies (telerehabilitation) has been adopted rapidly during the COVID-19 pandemic, and may be the key to overcoming many of these barriers.

A hybrid model of in-person and telerehabilitation, delivered either in-centre or in the home, is the most likely method of delivering effective pulmonary rehabilitation in a post-COVID-19 world Pulmonary rehabilitation in a post-COVID-19 world Wen et al.

In the pre-COVID-19 world, remote pulmonary rehabilitation was seen as a means of overcoming many of the known barriers to successful pulmonary rehabilitation. Poor access to pulmonary rehabilitation remains a problem: a global survey from 2013 found that less than 1.2% of people with COPD had reasonable access to pulmonary rehabilitation programs in their residential communities [17] . Even in highly developed countries, access is poor in rural communities [18,19 && ]. Low participation and completion rates are also issues, driven by factors, such as travel barriers, a perceived lack of benefit [20] , and physical challenges of regular participation [21] , all of which could potentially be addressed by delivering remote pulmonary rehabilitation. One of the biggest challenges for pulmonary rehabilitation is that there is a gradual decay of benefits after completing the program. This may be mitigated by implementing postpulmonary rehabilitation follow-up at home or back in the hospital. However, currently, only 22% of pulmonary rehabilitation programs in Canada offer an institutionally based maintenance component [17] . It is important to remember that these challenges existed before, and will likely persist beyond, the COVID-19 pandemic.

During the COVID-19 pandemic, in-person pulmonary rehabilitation programs were mostly halted to reduce the spread of the virus [22] . This has subsequently led to an increase in demand for pulmonary rehabilitation during the pandemic rapidly transitioned their Grosbois service to a program consisting of one supervised (via phone or video call) 90-min exercise session per week for 8 weeks. The completion rate was 79%, and there were significant improvements in both physical and psychological domains in the cohort as a whole. Interestingly, improvements in anxiety, depression, and fatigue were only observed in the subgroup of patients without COPD (n ¼ 34), which led the authors to speculate that face-to-face visits might play a more important role in pulmonary rehabilitation of COPD patients than other CRDs.

With approximately one-third of COVID-19 survivors suffering from a post-COVID-19 syndrome (often referred to as 'long COVID'), many patients who recover from their acute COVID-19 illness may also require pulmonary rehabilitation. There is no clear consensus definition of long COVID but an increasing number of studies has shown that this syndrome may affect several organ systems reported a single-centre case series of tele-pulmonary rehabilitation in three COVID-19 patients. In this 6-week program, all assessments were conducted remotely by video conferencing, and exercise was self-monitored using a pulse oximeter. The program led to improvements in exercise capacity and breathlessness in all three patients, as well as improvements in self-confidence and feelings of support during the recovery phase of COVID-19. Li et al. [32 && ] performed a multicentre RCT of a 6week unsupervised home-based pulmonary rehabilitation program, compared with a control group receiving educational sessions only, in previously hospitalized COVID-19 patients with residual dyspnoea. The investigators monitored the participants' heart rate and pulse oximetry remotely using a smartphone app. The intervention group demonstrated improvements in their functional exercise capacity, limb muscle strength, and physical HRQoL that were sustained over 7 months of follow-up but improvements in dyspnoea were short lived.

On the basis of the available evidence, pulmonary rehabilitation appears to be effective for COVID-19 survivors. A scoping review based on 40 most recent studies of pulmonary rehabilitation in COVID-19 patients suggested that pulmonary rehabilitation program should begin during patient's inpatient-stay alongside other medical interventions, and continue in an outpatient setting, either at a community centre or at home [33 & ]. Although the long-term consequences of COVID-19 in patients with and without COPD are unclear at this time, recent studies suggest that pulmonary rehabilitation could play a major role in restoring the functional status of these patients and improving their overall quality of life. Given that ''functional recovery and return to society are the ultimate medical outcomes instead of negative virology tests and the control of pulmonary inflammation'' [28], there is a pressing need to develop, coordinate, and enhance the healthcare framework and response, such as pulmonary rehabilitation, to support COPD patients during the pandemic.

With the rapid advancement in science and technology, various remote rehabilitation approaches are quickly evolving, ushering in a new era of 'smart rehabilitation'. Figure 1 shows the transitions through the pulmonary rehabilitation program preceding, during, and succeeding COVID-19, as well as the advantages and disadvantages of different modalities. Rigorous evaluation and clinical studies will be required to determine which of these approaches are clinically feasible and most importantly improve the outcomes and care of patients with COPD. Promisingly, the data to date suggest that tele-pulmonary rehabilitation is noninferior to conventional pulmonary rehabilitation programs, though most of the studies have been small in size and scope [34] .

The preferred model of delivery will be determined by infrastructure and expertise of individual centres and the needs of their patients. Programs may be supervised (i.e. an instructor guides the patient through the program) or unsupervised (i.e. self-guided, with the patient following a set routine

Hospital-based PR program or set of instructions), and the setting may be homebased or community-based. Given the success of its implementation during the COVD-19 pandemic period, a 'hybrid' model combining traditional pulmonary rehabilitation with remote tele-pulmonary rehabilitation may be the most desirable.

Bhatt et al. [35] recently reported outcomes from a live-monitored home-based pulmonary rehabilitation program offered to patients who were unable to attend a centre-based program. The investigators retrospectively matched participants to patients who had undergone conventional centre-based pulmonary rehabilitation; this allowed them to compare the two models, which had similar structures. They found that supervised tele-pulmonary rehabilitation produced similar clinical improvements to the centre-based program, suggesting that this is a viable alternative for patients who cannot participate in centre-based programs. Similarly, a recent multicentre RCT [36, 37] compared a supervised tele-pulmonary rehabilitation program, delivered over 10 weeks via video conferencing using basic exercise equipment, to a conventional centre-based pulmonary rehabilitation program. The two groups showed similar improvements in exercise capacity (6MWD), but the supervised tele-pulmonary rehabilitation group showed better completion rates. This suggests that tele-pulmonary rehabilitation may improve adherence to, and accessibility of, pulmonary rehabilitation programs. However, in both the tele-pulmonary rehabilitation and conventional pulmonary rehabilitation groups, the exercise improvements were not sustained over time. Tele-pulmonary rehabilitation programs present an opportunity to engage and maintain contact with patients so that the benefits of pulmonary rehabilitation may persist after completion of the program, but they require optimization to achieve this goal [38] .

Compared with a home-based model, communitybased tele-pulmonary rehabilitation programs may provide participants an environment for social interaction and peer support, both of which are valued by COPD patients [39] . Other advantages, such as not needing to create a dedicated space at home, make community-based models particularly attractive.

Alwakeel et al. [40 && ] implemented a provincewide community-based tele-rehab program in Quebec, Canada, at seven tele-sites (primary and secondary healthcare centres). All components of the 8week program were standardized by concurrently video-conferencing the standard pulmonary rehabilitation program delivered at the hospital (which served as the control group) to all the tele-pulmonary rehabilitation sites. At each tele-pulmonary rehabilitation site, one healthcare professional was present to set up and coordinate the video conferencing, and to ensure participants' safety. Improvements in exercise capacity and overall wellbeing were comparable with the standard pulmonary rehabilitation program. However, the combined tele-pulmonary rehabilitation group showed a higher completion rate (83 vs. 72%) and more sustained improvements in 6MWD and COPD Assessment Test (CAT) scores over 12 months. The investigators hypothesized that stronger, ongoing community support and reinforcement improved patients' self-management skills, and in turn their overall health status.

In an unsupervised tele-pulmonary rehabilitation model, patients undertake their own exercise training sessions and are followed-up with home visits or phone calls from health professionals to check on their progress and provide feedback [41] . Homebased unsupervised tele-rehab has been proposed as an alternative model that can increase access and lower the healthcare cost burden.

The outcomes from unsupervised home-based models appear to be mixed. For example, Benzo et al. [42] implemented a model of telephone health coaching along with unsupervised, video-guided exercise six times per week. This model showed a high degree of acceptability and adherence, as well as improvements in participants' self-management abilities, but no significant improvement in dyspnoea. Galdiz et al. [43] conducted a 12-month RCT comparing unsupervised tele-rehab program as a maintenance strategy to usual care (no intervention), and found that significant improvements were observed in psychological domains (SF-36, CRDQ-emotion score) but not exercise capacity.

The discrepancy in outcomes across different studies might be attributed to the contextual heterogeneity of these studies as there is no universally agreed upon standard for unsupervised pulmonary rehabilitation program. On top of that, there is a scarcity of literature comparing unsupervised telerehab to conventional pulmonary rehabilitation program. Therefore, more clinical studies are needed on this topic to fill this critical gap in knowledge and generate data to ensure the safety of participants in this setting.

Virtual reality allows users to experience an immersive, interactive, and multisensory computer-simulated 3D environment, which can reduce negative sensations [44] and make participants feel more engaged and motivated [45] . Virtual reality is, therefore, particularly attractive for rehabilitation programs, and has been successfully used for cognitive rehabilitation of poststroke patients [46] , motor rehabilitation of frail elderly patients [47] , gait training for individuals with Parkinson's disease [48] , as well as physical and cognitive training for older adults with mild cognitive impairment [49] . In all these settings, virtual reality-incorporated rehabilitation achieved comparable or better results compared with traditional methods of rehabilitation delivery.

There are some recent trials using virtual reality as part of pulmonary rehabilitation programs for COPD patients. One RCT used immersive virtual reality therapy as a supporting method for COPD patients who were undergoing hospital-based pulmonary rehabilitation. This program showed benefits in reducing stress levels and improving symptoms of depression and anxiety compared with the control group, which received traditional therapeutic training [50] . The same research group also investigated and demonstrated that virtual reality training can improve exercise tolerance [51] and physical fitness [52 & ] in COPD patients. A pilot study demonstrated that a remotely supervised virtual reality-based pulmonary rehabilitation program effectively improves participants' physical ability, psychological well being, and their HRQoL [53 && ]. In this study, the virtual reality technology enabled health practitioners to track and monitor patients' physiological performance data, which increased patients' confidence and ensured their safety during exercise. A review on virtual reality application for COPD rehabilitation from a technological perspective has also shown that the use of virtual reality can be a promising solution to improve both at-home and in-hospital pulmonary rehabilitation [54] but there are still many aspects that have not been fully investigated. These include some side effects of virtual reality, such as dizziness that prohibit its application in some patients and reduce the long-term effectiveness of virtual reality in improving patient outcomes.

Despite increasing evidence for the feasibility and safety of remote tele-pulmonary rehabilitation, a 'hybrid' pulmonary rehabilitation model may be more desirable as some in-person components may be indispensable. For example, initial assessment and exercise prescription have been performed in-person in most tele-pulmonary rehabilitation programs, either incentre [35,40 && ] ]. Many tele-pulmonary rehabilitation studies did not specify how the exercises were prescribed in the virtual setting, making it difficult to compare studies. In one small case series, initial assessment and exercise prescription were performed via video conferencing with the patient in full view [31] . Larger studies are required to determine whether the virtual exercise prescription is appropriate and can achieve maximal benefits.

More research is needed to ascertain the optimal methods for delivering telemedicine for patients with COPD in the community based on patients' needs and preferences, as echoed in a recent ATS Workshop report [19 && ]. For example, a recent feasibility and acceptability trial [55] using a web-based pulmonary rehabilitation platform (SPACE) in patients who had experienced a recent acute exacerbation of COPD (AECOPD) reported technological barriers that led them to 'give up' on the program as they could not navigate the website. This, in turn, reduced their motivation to exercise. Guidelines and further clinical evidence are needed to optimize pulmonary rehabilitation programs suited for different patient populations. The cost-effectiveness of implementing telepulmonary rehabilitation remains unknown as there is scarcity of literature on the topic. Barbosa et al. [34] recommended that future clinical trials include a cost analysis, which can provide financial insights and be used for reimbursement and/or investment into these programs. It should be noted that telemedicine is heterogeneous in its infrastructure and delivery, which poses difficulties for quantitative analysis and generating standards/guidelines in the field. There are some recommendations in terms of the components, which should be incorporated in future studies ( Table 2) to fill the gap in knowledge and to promote the creation of guidelines.

The COVID-19 pandemic has changed our lives drastically and forced the healthcare system to shift its focus to virtual care delivery. This shift has brought the tele-pulmonary rehabilitation to the centre stage and demonstrated its value as a viable alternative to face-to-face delivery of pulmonary rehabilitation. Greater-scale adoption of tele-pulmonary rehabilitation into the medical community will happen gradually, and multidisciplinary collaboration, along with high-quality clinical studies, and technology advancement are the keys in supporting and accelerating this process [56] . The most important reason for the lack of success in sustaining the benefits of pulmonary rehabilitation over time in patients is the failure to fully embed a regular exercise routine into patient's daily life and, as a result, patients returned to their sedentary lifestyle shortly after completion of the pulmonary rehabilitation program. Ultimately, the goal of achieving a tailored patient-centred pulmonary rehabilitation program is to understand individuals' daily life and to figure out the best exercise routine for each of them. This study is notable as it includes cohorts of COPD and non-COPD respiratory patients, and that improvements in anxiety and depression were not significant in the COPD cohort. This supports an individualized approach to pulmonary rehabilitation, where a hybrid model combining some in-person rehabilitaion may be more suitable for COPD patients. This observational study is particularly important as it highlights the risk of developing 'long COVID' even in younger people with mild disease. The implications of these finding are that an age cohort not usually seen in pulmonary rehabilitation may require this service as the pandemic progresses. 30. 

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This study is impressive in its size and scope, being conducted province-wide and demonstrating how a tele-pulmonary rehabilitation model can be successfully implemented at a health system level

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None.

There were no direct financial sponsors for the submitted work. J.W. and S.M. were supported by the MITACS Accelerate program. D.D.S. is a Tier 1 Canada Research Chair in COPD, and the De Lazzari Family Chair at the UBC Centre for Heart Lung Innovation.

There are no conflicts of interest.

Papers of particular interest, published within the annual period of review, have been highlighted as: & of special interest && of outstanding interest