key: cord-0979089-zonv6csa
authors: Tsutsui, Mai; Gerayeli, Firoozeh; Sin, Don D
title: Pulmonary Rehabilitation in a Post-COVID-19 World: Telerehabilitation as a New Standard in Patients with COPD
date: 2021-02-19
journal: Int J Chron Obstruct Pulmon Dis
DOI: 10.2147/copd.s263031
sha: 30f7b9ad10a21b27a7fd37fbb903cb5c2e40f758
doc_id: 979089
cord_uid: zonv6csa

Pulmonary rehabilitation (PR) is effective in reducing symptoms and improving health status, and exercise tolerance of patients with chronic obstructive pulmonary disease (COPD). The coronavirus disease 19 (COVID-19) pandemic has greatly impacted PR programs and their delivery to patients. Owing to fears of viral transmission and resultant outbreaks of COVID-19, institution-based PR programs have been forced to significantly reduce enrolment or in some cases completely shut down during the pandemic. As a majority of COPD patients are elderly and have multiple co-morbidities including cardiovascular disease and diabetes, they are notably susceptible to severe complications of COVID-19. As such, patients have been advised to stay at home and avoid social contact to the maximum extent possible. This has increased patients’ vulnerability to physical deconditioning, depression, and social isolation. To address this major gap in care, some traditional hospital or clinic-centered PR programs have converted some or all of their learning contents to home-based telerehabilitation during the pandemic. There are, however, some significant barriers to this approach that have impeded its implementation in the community. These include variable access and use of technology (by patients), a lack of standardization of methods and tools for evaluation of the program, and inadequate training and resources for health professionals in optimally delivering telerehabilitation to patients. There is a pressing need for high-quality studies on these modalities of PR to enable the successful implementation of PR at home and via teleconferencing technologies. Here, we highlight the importance of telerehabilitation of patients with COPD in the post-COVID world and discuss various strategies for clinical implementation.

The severe acute respiratory syndrome coronavirus 2 (SARS-Cov-2) is a novel betacoronavirus 1,2 that was first identified in December of 2019 through a cluster of pneumonia with an unknown origin. 2, 3 The disease caused by this virus is now known as Coronavirus disease , and has been characterized as a global pandemic by the World Health Organization since March 11th 2020. SARS-CoV-2 shares 80% sequence homology with its original counterpart SARS coronavirus that led to an outbreak in 2003. 1,2 SARS-CoV-2, however, has evolved features that have enhanced its ability to bind to its receptor, angiotensin-converting enzyme-2 (ACE-2) on the cell surface and to penetrate inside the cells, causing cellular infection. 4, 5 The clinical manifestation of COVID-19 ranges from no symptoms to life-threatening pathologies, such as vasculitis, myocarditis, severe pneumonia, multi-organ failure, and death. 1, 6 Although the virus attacks most frequently the respiratory tract, COVID-19 can directly and indirectly through cytokine storms or vascular inflammation and thrombosis lead to many non-pulmonary complications. 6, 7 Chronic obstructive pulmonary disease (COPD) is a condition that is characterized by persistent airway inflammation and airflow limitation. 8 It is the 3rd leading cause of mortality worldwide. 8, 9 There is an ongoing controversy on whether COPD is a risk factor for COVID-19. Although some have reported an increase in the risk, 10, 11 other studies have shown no significant association; 12 and a few studies have even reported a protective relationship. 11, 13, 14 As most of these studies have relied on self-report or a physician diagnosis of COPD, which is prone to measurement error, diagnostic misclassification may in part explain the variation in the results across these studies.

Studies of patients with severe COVID-19, however, have produced more consistent results. While there is still some variation in data, the totality of results indicates that COPD is a significant risk factor for severe COVID-19, increasing the risk by 50% to 100% and leading to poor outcomes including longer stays in the intensive care unit (ICU) and mortality. 10, 15 The reason for this observation is unclear. One possibility is that COPD patients have poor lung function reserves, 16 which when challenged with SARS-CoV-2 pneumonia may lead to respiratory failure and death. Another possibility is the significant upregulation of the ACE-2 receptor in the small airway epithelium of individuals with COPD. 17, 18 As noted previously, SARS-CoV-2 primarily uses ACE-2 as its cognate receptor to invade cells in the respiratory tract. ACE-2 expression levels are highest in the nasal cavity and progressively decrease as the airways branch and become smaller in size. 19 ACE-2 expression is generally very low in the gas exchange units of the lung. 19 However, with COPD, airway expression levels of ACE-2 increase, even in the small airways 17 This may allow the virus to propagate from the upper airways into the smaller airways, causing pneumonia. Once the lower airways become infected with the virus, the host down-regulates ACE-2, which may limit the spread of the virus. 20 However, the "side effect" of this process is local vasoconstriction, and inflammation, which increases the risk of complications, such as diffuse alveolar damage, vascular endothelialitis, thrombosis, and hypoxemia. 21 A third possibility is that in COPD patients, there may be up-regulation of ACE-2 in the myocardium. 22 This may enable the virus to directly infect the heart and cause myocardial damage. 23 Patients with severe COVID-19 experience a considerable amount of morbidity during hospitalization. Many of these deficits including lethargy, breathlessness, diffuse myalgias and cognitive dysfunction may remain post-recovery from the acute illness. 24, 25 Approximately 50% of patients with severe COVID-19 will require rehabilitation following hospital discharge. [26] [27] [28] However, owing to constraints of social and physical distancing and concerns over SARS-CoV-2 transmission in the community, traditional modes of rehabilitation cannot be easily implemented during the pandemic. Here, we will discuss the PR for COPD patients in the COVID-19 era with a perspective of finding a new standard of PR delivery. 29, 30 

Pulmonary rehabilitation (PR) is one of the most effective management strategies to improve shortness of breath, health status, and exercise tolerance of patients with COPD. It also leads to a reduction in symptoms of anxiety and depression. Many randomized controlled trials, metaanalyses, and evidence-based reviews have provided solid evidence for the benefits of PR programs in symptomatic COPD patients. 8, 31 The 2013 American Thoracic Society (ATS)/European Respiratory Society (ERS) Statement defines PR as a comprehensive intervention based on a thorough patient assessment followed by patient-tailored therapies, which include, but are not limited to, exercise training, education, and behavior change, designed to improve the physical and emotional condition of people with chronic respiratory disease and to promote the long-term adherence of healthenhancing behaviors. 32 More broadly, PR is considered as a critical component of integrated patient management, and usually includes a range of healthcare professionals to ensure optimal outcomes. 33 The multidisciplinary team for PR generally consists of pulmonologists, physical medicine specialists, social workers, psychologists, nurses, respiratory therapists, occupational therapists, physiotherapists, general practitioners, pharmacists, and dieticians. Patients with a high symptom burden or those at increased risk of exacerbations are recommended to participate in a formal submit your manuscript | www.dovepress.com

International Journal of Chronic Obstructive Pulmonary Disease 2021:16 380 rehabilitation program that is structured and multidisciplinary. 34, 35 PR Before COVID Although there is tremendous variation in the structure and setting of PR across the world, the most common form of PR is implemented through an outpatient, hospital-based exercise program. According to a global survey completed by representatives of 430 centers from 40 countries, 262 (60.9%) were outpatient programs while 41 (9.5%) were inpatient programs, and 106 (24.7%) centers offered both. Only 21 (4.9%) programs were based at home or in a primary care setting. 36 It should be noted that, to date, most of the evidence supporting the benefits of PR have been generated from studies or PR programs that were hospital-based. [37] [38] [39] Three major US and international guidelines recommend that, for optimal therapeutic benefits, a PR program should consist of at least 3 to 5 supervised (exercise) sessions per week for 12 weeks (of at least 20 minutes per session) during which patients achieve >60% of maximal peak exercise capacity. 33, 37, 39 Optimally, PR sessions should include endurance training, interval training, and resistance/strength training of upper and lower limbs in addition to walking exercises. Other key components of PR include self-management training. Self-management interventions are structured, often multi-component, and ideally personalized to achieve goals of patient motivation, and engagement to enable adoption of positive health behaviors and development of self-management skills and mastery of their disease. 40 Randomized controlled studies (RCTs) have shown that self-management interventions when properly implemented improve patients' health status and decrease their risk for hospitalization and emergency department visits. [41] [42] [43] [44] However, despite the known benefits of PR, in the real world, patients' attendance and completion rate of PR are low. For example, in 2018, Keating et al reported in a systematic review that the percentage of referred participants who did not attend any PR sessions ranged from 8.3% to 49.6% and the percentage of non-completers ranged from 9.7% to 31.8%. The major barriers to PR compliance were 1) disruption to patients' established routine; 2) a lack of enthusiasm for PR by patient's physician; 3) a lack of perceived benefit, and 4) inconvenient timing. An often overlooked impediment is transportation. Indeed, some studies have shown that insufficient transportation to and from hospital-based PR programs to be the most common barrier to participation in PR. 45, 46 It has been reported that those who travelled more than 30 minutes to a PR center were significantly less likely to complete PR than those who travelled shorter distances. 47, 48 The authors of this review concluded that to enhance uptake and completion of PR programs, more attention is required to remove these barriers by subsidizing transportation, providing greater support for patients in enrolling and completing PR, and empowering patients to make informed decisions about their care. 49 In 2015, the Official ATS/ERS Policy Statement on Enhancing Implementation, Use and Delivery of PR 50 highlighted other common barriers to PR: insufficient funding for the programs; limited resources for PR programs; inadequate reimbursement for PR; a lack of awareness and knowledge of the benefits of PR by healthcare professionals, payers, patients, and caregivers; suboptimal use of PR by suitable patients; 46,51 and limited training opportunities for PR professionals.

One method of addressing some of these gaps in care is by instituting home-based PR programs. There is a growing body of evidence to suggest that home-based exercise training is feasible and can be effective in improving exercise capacity, reducing breathlessness, and enhancing quality of life. Notably, home-based programs can significantly improve patients' adherence and completion rates to PR. 31,52-57 Maltais et al, for example, conducted an RCT of 252 patients with moderate to severe COPD in 10 academic and community medical centers across Canada. The study assessed whether self-monitored, home-based rehabilitation was as effective as outpatient, hospital-based rehabilitation in these patients. They found that home rehabilitation was non-inferior to hospital-based outpatient programs in patients with COPD. 52 Mccarthy et al performed a meta-analysis and found that home-based PR resulted in significantly greater improvements in exercise capacity and health-related quality of life (HRQoL) compared with usual care in patients with COPD. 31 Importantly, as outlined by Bourbeau et al, 57 for optimal results, a home-based PR program must be capable of preserving all core components that define PR, including exercise program supervision, a multidimensional approach, and education with self-management interventions.

Another method of addressing the limitations of traditional hospital-based PR programs is through telerehabilitation. 28,58,59 Telerehabilitation (a subset of telehealth) is the use of information and communication technologies to provide clinical rehabilitation services from a distance. 60 It can be provided in a variety of different ways, including two-way real-time visits with audio, video, or both; asynchronous e-visits; virtual check-ins; remote evaluations of recorded videos or images; or telephone assessment and management services. 61 It may be delivered directly to a patient's home or a nearby healthcare facility. 62 The common approach of building an information technology (IT) infrastructure to support telerehabilitation is to purchase IT systems that create similar experience as that which is experienced through traditional face-to-face encounters. Some examples of these IT infrastructure include a videoconferencing system, virtual reality, and electronic/ portable devices. 63 Essential telerehabilitation technology components include human factors (patients, providers, organizations, and society), economic factors, and technologies. 64 The various components of telerehabilitation are shown in Figure 1 .

The earliest publication of telerehabilitation can be traced back to 1998. 65 Since then, the use of technology in homebased telerehabilitation has gradually increased as an alternative to the conventional hospital-based PR. Telerehabilitation is currently used primarily in cardiac, musculoskeletal, and neurological rehabilitation. 58, 66 There have been a number of telerehabilitation studies in COPD. [67] [68] [69] [70] [71] [72] [73] [74] [75] [76] Two pilot RCTs evaluated a web-based exercise program consisting of smartphone activity coaching, self-management education, and teleconsultations compared with a control group that consisted of usual care. 67, 68 These studies showed that web-based rehabilitation program was associated with improvements in activity level, higher compliance to the activity coaching, 65 and increased patient satisfaction with the exercise program. 68 Tsai et al conducted an RCT in patients with COPD to determine the effects of home-based telerehabilitation that incorporated direct supervision of all exercise sessions using real-time videoconferencing. They found that this approach significantly improved exercise endurance and self-efficacy of patients. There was also a positive trend towards improvements in health-related quality of life (HRQoL) when compared with usual medical care. 74 Recently, Hansen et al conducted a single-blinded, multicenter RCT that investigated the effects of a supervised telerehabilitation program (PTR) compared with a supervised conventional PR program. The authors hypothesized that telerehabilitation would be superior to a supervised conventional PR in improving 6 min walk distance, possibly by increasing patients' adherence rate to the program. The telerehabilitation method was given via a videoconferencing software system that was implemented through a single touch screen. The investigators however failed to find a significant difference in outcomes between PTR and conventional PR; interestingly, more participants completed PTR. 75 There is another assessorblinded, multi-center RCT that is evaluating the effectiveness of home-based telerehabilitation versus traditional center-based pulmonary rehabilitation in patients with COPD (the REAcH trial); 77 the results are pending. In summary, while there have been several clinical studies of telerehabilitation including RCTs, its implementation in the community has been slow and variable. 78, 79 Studies 67-75,77 of telerehabilitation in COPD are shown in Table 1 . There is tremendous heterogeneity in the design of these studies including measurement of clinical outcomes, such as activity level, endurance time in walking, and the number of hospital admissions pre-and post-PR and the technologies that were deployed in these studies.

COVID-19 pandemic has greatly impacted all aspects of health care delivery. Precautions related to COVID-19 have created a need for safer service delivery options for health services. To protect health care workers and patients across the country from disease transmission, rules, regulations, and reimbursement policies have been substantially altered to enable widespread use of telecommunications technology in lieu of in-person clinical visits. 80 In response to this new landscape of medical practice, multiple organizations, such as the American Physical Therapy Association, Australian Physiotherapy Association, and Italian Physiotherapy Association, have expanded resources and advice for the implementation of telerehabilitation services.

According to the Report from the American Physical Therapy Association published in June 2020, 81 physical therapy services have been deemed as essential by federal, state, and local authorities during the pandemic. Despite this, many physical therapists have proactively curtailed their hours of work to reduce patient contact time to "flatten the curve" of the pandemic. Overall, 54% of physiotherapists (PTs) have reduced their work-time and only 10% have increased their work-hours.

The American Physical Therapy Association recommends the implementation of video-conferencing technology to enable direct communication between PTs and clients during the pandemic. Prior to the pandemic, 98% of PTs surveyed were not providing live video consultations. Of the 2% who were, the vast majority (69%) reported seeing less than one patient per week.

During the pandemic, 50% reported providing live video consultations. Of these, just over half (51%) treated between one and five patients per week, 17% treated six to 10 patients per week, and 17% treated more than 10 patients via live consultations. In terms of delivery, the most popular platform for video consultations was Zoom ® , which was endorsed by 43% of the PTs, who participated in the survey. Doxy.me ® was used by another 30%, and Epic ® was used by 9%. Respondents identified more than two dozen platforms that were used to facilitate video-based care. Notably, 31% of those surveyed said that their patients and clients lacked adequate technology, and 21% said their facility's technology was a limiting factor in delivering e-technologybased care.

As COPD patients are particularly vulnerable to severe complications of COVID-19, in-person PR should not be conducted during the pandemic, except in exceptional circumstances. 82, 83 In-person PR may be considered only when the community spread of COVID-19 is low. For those PTs, who must provide in-person care during the pandemic, acceptable personal protective equipment (PPE) should be worn at all times. Despite these recommendations, several dozens of those surveyed commented that they found their PPE supplies to be inadequate. 81 One study found that 67% of PTs were provided PPE training by their employer since the advent of the pandemic; 8% reported not being provided PPEs, while 18% had to cancel appointments with their clients because they lacked PPEs. The Canadian Thoracic Society has identified several factors that are critical to reducing the risk of virus transmissions. This includes screening procedures for in-person PR, sufficiently large exercise space (to enable social distancing), equipment preparation and regular cleansing, and proper use of waiting areas. Hybrid models that include in-person assessment and exercise testing, and a combination of inperson and virtual exercise training, education, and selfmanagement can be used to optimize exercise safety and training effectiveness while decreasing the risk of disease transmission and infection rates. 84 It should be noted that modern telerehabilitation technologies should contain devices that will enable remote monitoring of physiological signs and symptoms during exercise in real-time or in a "store and forward" capacity. There should also be the ability for supervisors to "beam-in" when necessary to provide instant feedback to the 

Despite the rapid progress of telerehabilitation, there are still many challenges and impediments to its widespread adoption in the community. Prior to the COVID-19 pandemic, the use of telerehabilitation was low (~4.9% including all home-based PR). 70 One major impediment is the lack of well developed, evidence-based statements to guide its set-up in the community. Another major impediment is a paucity of high-quality evidence indicating that telerehabilitation confers comparable or even greater clinical benefits to patients compared with traditional programs at a reasonable (or lower) cost. 50, 74 There is also a pressing need to understand which patients, if any, benefit the most from telerehabilitation. 86 While there have been a number of telerehabilitation studies in COPD, 67, 75 the contextual heterogeneity of these studies (including the type of intervention, the participants involved, and the health care system in which they were deployed) makes clinical implementation extremely challenging. 85 Since the introduction of telerehabilitation can be quite expensive, it is important to ensure that its implementation is grounded on sound clinical policy decisions and solid high-quality evidentiary data. If these challenges can be addressed, telerehabilitation holds great "therapeutic" promise for a large number of COPD patients during and post-COVID-19 pandemic. 55 In most jurisdictions, telerehabilitation is poorly funded. Funding is important to build a solid foundation of evidence for its use and to enable the sustainability of these programs in the community. Before the COVID pandemic, many insurers around the world were willing to reimburse PR in the outpatient setting but not for telerehabilitation. 85 , 87 Bierman et al reported in 2018 that the uptake of telerehabilitation in health systems across the United States was hampered by variation and restrictions in state regulations and reimbursement policies of Medicare and private insurers. 87 Legislation providing funding for telerehabilitation would provide a permanent policy solution to expand its use in the community.

There are also challenges related to access and use of technology, optimal mode of assessment, and the ability to obtain outcome measures, as well as adequate supervision of patients during PR. During the pandemic, patients have Cox 75, 81, 88 have found that people with less experience in digital technologies, such as the elderly population, were less likely to enjoy PR programs and thus more likely to leave the program. This is relevant for COPD patients, who tend to be older. Recently, Bentley et al developed a smartphone app and an activity tracker to help people with COPD to maintain (or increase) physical activity after undertaking PR. Their RCT showed that simplicity and usability of the technology were the two most important determinants of patient engagement with the intervention. 89 It is not known whether PR adherence improves by adding online (support) groups to the videoconferencing technology. 75 Remote assessment may be difficult, as the current technology does not fully enable "physical examination" of patients. This may limit the caregivers' ability to establish an accurate functional status at baseline for the patient, and to prescribe the "right" intensity and duration of PR for the patient to achieve optimal outcomes. As there is no current technology that can ensure the safety of patients during unsupervised PR, adequate supervision from trained PR healthcare professionals is still necessary at this moment. Technology that enables accurate evaluation of remote PR and ensure the safety of patients in unsupervised settings is eagerly anticipated. Another current limitation is that in many jurisdictions, there is a shortage of qualified health professionals, who are trained in home-based PR or telerehabilitation. 33 The COVID-19 pandemic has resulted in a dramatic change in our community and many losses of lives. These changes as well as barriers to pulmonary rehabilitation for COPD patients are summarized in Figure 2 . Although traditionally PR has been hospital or cliniccentered, the pandemic has prompted discussions and debates on the merits of home-based PR as well as telerehabilitation. There is now a pressing need for highquality studies on these modalities of PR to enable successful implementation of PR but supervised and unsupervised at home and via teleconferencing technologies.

SARS-Cov-2, severe acute respiratory syndrome coronavirus 2; COVID-19, Coronavirus disease 19; ACE-2, angiotensinconverting enzyme-2; COPD, chronic obstructive pulmonary disease; PR, pulmonary rehabilitation; RCTs, Randomized controlled studies; ATS, American Thoracic Society; ERS, European Respiratory Society; IT, information technology;

Practical changes and barriers in pulmonary rehabilitation for COPD patients in the post-COVID world. The COVID-19 pandemic has resulted in dramatic changes in the way in which pulmonary rehabilitation (PR) is delivered. These include changes in venue and increased use of telerehabilitation. The pandemic has also revealed the long-standing structural barriers of PR, such as the lack of financial support, resources, and healthcare professionals, which have been exacerbated during the COVID pandemic. HRQoL, health-related quality of life; PTR, telerehabilitation program; PPE, personal protective equipment.

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All authors made substantial contributions to conception and design, acquisition of data, or analysis and interpretation of data; took part in drafting the article or revising it critically for important intellectual content; agreed to submit to the current journal; gave final approval of the version to be published; and agree to be accountable for all aspects of the work.

The authors report no conflicts of interest in this work.