From Inception to Implementation: Strategies for Setting Up Pulmonary Telerehabilitation

Background: The emergence of innovative technology-enabled models of care is an opportunity to support more efficient ways of organizing and delivering healthcare services and improve the patient experience. Pulmonary telerehabilitation started as a promising area of research and became a strategic pandemic response to patients' decreased accessibility to rehabilitation care. Still, in the pre-COVID-19 era, we conducted a participatory study aiming to develop strategies for setting up pulmonary telerehabilitation as a person-centered digitally-enabled model of care.

Methods: We performed operational participatory research between June 2019 and March 2020 with the engagement of all stakeholders involved in the implementation of pulmonary telerehabilitation, including 14 people with Chronic Obstructive Pulmonary Disease. Patients were assessed subjectively and objectively pre and post a 3-month pulmonary rehabilitation program including exercise and education, which started in a face-to-face hospital setting during the first month and continued as a home-based, remotely supervised exercise training intervention.

Results: Five major groups of requirements targeted operational strategies for setting up pulmonary telerehabilitation: (1) pulmonary rehabilitation core principles, (2) quality and security standards, (3) technological functionality, (4) home environment appropriateness, and (5) telesetting skills. There was a statistical significance in the median change in the CAT score from 15.5 to 10.5 (p = 0.004) and in the PRAISE score from 49.5 to 53.0 (p = 0.006). Patients' mean levels of satisfaction regarding rehabilitation goals achievements were 88.1 ± 8.6% and the mean levels of satisfaction regarding the telerehabilitation experienced as a model of care were 95.4% ± 6.3%.

Conclusions: The success of telerehabilitation implementation was grounded on stakeholder engagement and targeted strategies for specific setup requirements, achieving patients' high satisfaction levels. Such operational experiences should be integrated into the redesigning of upgraded telerehabilitation programs as part of the solution to improve the effectiveness, accessibility, and resilience of health systems worldwide.

Introduction

Over the last decade, the progressive adoption of technology in healthcare has brought about a significant revolution in health service delivery and in the interactions between patients and healthcare providers (1). Pulmonary rehabilitation, as a comprehensive patient-tailored intervention including exercise training, education, and behavior change, faces the ultimate challenge of succeeding in improving patients' long-term adherence to health-enhancing behaviors (2). To optimize such a purpose, the strategy of providing a real-life setting by means of home-based programs with remote supervision comes as a realistic rationale, as it might increase both patient engagement and pulmonary rehabilitation responsiveness with enduring effectiveness in everyday life. As an add-on, the emergence of innovative technology-enabled models of care presents new and exciting opportunities (3) where telerehabilitation provides delivery of pulmonary rehabilitation programs either by means of a telephone, a website or mobile application, or via video-conferencing (4). With established scientific evidence (5–9), telerehabilitation in chronic respiratory disease presents similar outcomes compared to traditional in-person, center-based pulmonary rehabilitation (10).

While acknowledging that digital solutions enable more efficient ways of organizing and delivering healthcare services, it is of great importance that the design of such models of care meets the needs of people and health systems. Participatory research aims for the convergence of the perspectives of science and practice (11), empowering co-researchers to rethink established programs, services, and policies and enabling the co-creation of products the community can utilize (12). Beyond inception, innovative solutions through new technologies must be thoughtfully implemented to suit the local context, taking into account not only the best clinical practice but also organizational changes and, very importantly, improved patient experience. To succeed in such a purpose, the active engagement of all parties is essential, including patient involvement. Unaware of a challenging pandemic scenario to come, we conducted participatory research including patients within stakeholders, with the aim to develop strategies for setting up pulmonary telerehabilitation as a person-centered digitally-enabled model of care.

Materials and Methods

Operational participatory research with the engagement of all stakeholders involved in the implementation of pulmonary telerehabilitation is described in Table 1.

TABLE 1

Table 1. Participatory research framework.

Patient engagement included people with Chronic Obstructive Pulmonary Disease (COPD) referred for pulmonary rehabilitation at Hospital Pulido Valente in Lisbon, Portugal (June 2019 to March 2020). Participants had a confirmed COPD spirometry diagnosis and were stable without any clinical exacerbation or hospitalization in the previous 6 weeks. Exclusion criteria were uncertainty to commit with program adherence for 3 months; exercise-compromised clinical conditions (metastatic neoplasia, infectious or unstable cardiac diseases, osteoarticular, neuromuscular, unstable psychiatric or cognitive disorders); referenced candidate to lung transplant; multi-resistant bacterial infection/colonization; and any formal exercise contra-indications. Given the extenuating circumstance of COVID-19, which was declared a pandemic on 11 March 2020 by the World Health Organization, as defined by the CONSERVE 2021 Statement (13), ongoing research activity was affected. An important trial environment factor that was affected was the feasibility, as non-urgent clinical activity was suspended by the Board of the Hospital in line with national instructions by the Portuguese Directorate-general for Health. Suspended recruitment and exclusion of outcomes objective face-to-face evaluations were additional factors that directly impacted the trial. Mitigation strategies applied were the completion of the intervention phase for subjects already enrolled, and data collection was conditioned with remote subjective outcomes assessment. Despite the initial study design of patients randomly allocated either for a traditional face-to-face ambulatory pulmonary rehabilitation program (control group) or to a pulmonary rehabilitation program with telerehabilitation, given the described research limitations per-protocol suspension, this article presents a proof of concept with a randomized telerehabilitation group, leaving out the control group. The research was performed in accordance with the Declaration of Helsinki, with informed consent given prior to any proceeding. Ethical approval was obtained from the Ethics Committee of Centro Hospitalar Universitário Lisboa Norte, and Centro Académico de Medicina de Lisboa (number 43/17).

Patient clinical objective assessment was performed in accordance with the relevant guidelines and included: exercise capacity with a cardiopulmonary exercise test (14–16); functional capacity with the 6-min walk test (17–19) and the 1-min sit-to-stand test (20–22); daily activity functional capacity with the Glittre test (23–26) and a handgrip strength test (27–29). The subjective assessment included health-related quality of life by means of the EuroQoL 5 dimension Visual Analog Scale (30, 31) and the COPD Assessment Test (CAT) (32, 33); dyspnea with the modified Medical Research Council dyspnea scale (mMRC) (34) and the London Chest Activity of Daily Living scale (LCADL) (35, 36); anxiety and depression using the Hospital Anxiety and Depression Scale (HADS) (37); self-efficacy by means of the Pulmonary Rehabilitation Adapted Index of Self-efficacy Scale (PRAISE) (38, 39); and cognitive function by application of the Montreal Cognitive Assessment test (MoCA) (40, 41).

Pulmonary rehabilitation was designed as a 3-month group intervention with a multidisciplinary program (respiratory physician, physiotherapist, dietitian, and psychologist), including 6 self-management education sessions based on the Living-Well with COPD™ program (42) and 24 exercise training sessions supervised by the physiotherapist, as presented on Figure 1. The exercise training intensity was based on cardio-pulmonary exercise testing with an incremental protocol using a bicycle ergometer. Aerobic exercise training included modalities with a bicycle ergometer, treadmill, upper-limb ergometer, and rowing machine in the hospital face-to-face rehabilitation and bicycle and upper-limb ergometers domiciliary allocated for telerehabilitation. Aerobic exercise duration was 30–45 min, with targeted training intensities between 60 and 80% VO₂peak (43), initiated at the maximum tolerated intensity for a round of 10 continuous minutes had been accomplished with SpO₂ > 90% and a Modified Borg Scale score below 5 either for dyspnea or muscle fatigue. Progression was executed each session, increasing first the duration and then the intensity, according to patient tolerance. Strength exercise training included the use of weighted balls, dumbbells, and elastic bands for three exercises with three sets of 10 repetitions with breathing control and oximetry monitoring during pauses between sets to monitor SpO₂ > 90%. Flexibility training included four global muscle chain exercises on stall bars (posterior, anterior, and lateral) and specific stretching exercises according to the selected ergometers during the aerobic training (quadriceps, hamstrings, calf, biceps, triceps, pectoralis, and rhomboids). Also, at the end of each exercise session, there was a 10-min routine of laying down relaxation with dimmed light, soothing music, and guided breathing control.

FIGURE 1

Figure 1. From hospital face-to-face rehabilitation to home-based telerehabilitation.

Patients were enrolled in the program in a hospital setting during the first month and were upgraded to a home-based real-time monitoring video-call telerehabilitation after 3 months. The VSee platform (VSee, California, United States of America) was used for telerehabilitation, as it fulfilled the requirements of the General Data Protection Regulation and the Health Insurance Portability and Accountability Act; additionally, this was the official selection by the NASA Space Station to provide secure video conferencing. Baseline logistics for telerehabilitation were a hospital computer exclusive to telerehabilitation, including a webcam and earphones. Also, to enable telerehabilitation implementation without excluding patients that could not afford the expenses of the equipment, technology, and communication for remote care, each patient was provided for domiciliary usage a stationary bicycle (Domyos Essential 2 Bike, DECATHLON, China), an upper-limb cycle ergometer (YF612 minibike, Tecnovita—BH, Portugal), a digital oximeter (PRIM oximeter Md300C15D, PRIM, Spain), a blood pressure and pulse rate monitor (OMRON M2, OMRON Healthcare Co. Ltd., Japan), an android 4G tablet (Vodafone Smart TAB N8, Vodafone, China) including earphones and internet card, and a Borg scale. This represented an initial investment of 570€ per telerehabilitation kit, delivered and collected from each patient's home and continuously reallocated to new patients. Additionally, there were operating costs with data communication of 40€ per patient within the program aside from the hospital support provided by human resources and services.

When the pulmonary rehabilitation program concluded, patients used a scale from 0 to 100% to report their level of satisfaction with the rehabilitation goals achievement and their level of satisfaction with pulmonary rehabilitation with telerehabilitation experienced as a model of care.

Statistical analysis and data management were performed using the Statistical Package for the Social Sciences (SPSS) version 25.0 (SPSS Inc., Chicago, IL, USA). Descriptive statistics, such as frequencies, were presented as percentages, and data were expressed as median and interquartile ranges. Changes in pulmonary rehabilitation outcomes were analyzed by related-sample Wilcoxon Signed Rank test with a p-value of less than 0.05 being considered statistically significant.

Results

Table 2 presents baseline patient characteristics, including subjective and objective assessments.

TABLE 2

Table 2. Baseline patient characteristics.

The inception of this pulmonary rehabilitation model integrated telerehabilitation as a continuum of care after a hospital setting period of 1 month. This configuration was important to achieve crucial requirements for telerehabilitation implementation. According to a consolidated framework for advancing implementation science, there are five major domains that influence implementation effectiveness: the intervention, inner and outer settings, the individuals involved, and the process by which implementation is accomplished (44). As a result of stakeholders' participatory engagement in pulmonary telerehabilitation implementation, this study proposes five major groups of requirements for setting up pulmonary telerehabilitation, as presented in Figure 2: pulmonary rehabilitation (PR) core principles, quality and security standards, technological functionality, home environment appropriateness, and telesetting skills. If the first two groups comprise pulmonary rehabilitation classical requirements regardless of implementation setting, the last three groups are telerehabilitation specific and a tacit knowledge to be considered.

FIGURE 2

Figure 2. Requirements for setting up pulmonary telerehabilitation.

Core pulmonary rehabilitation principle requirements were developed through strategies such as the following: (1) in-person individual exercise response profile evaluation; (2) in-loco patient warm-up, exercise, and cool-down learning phases; (3) presential contact with a pneumologist, physiotherapist, dietitian, and psychologist during self-management education sessions; (4) patient group intervention with individually engagement and commitment to the program by socializing among peers; and (5) a face-to-face therapeutic relationship built with the physiotherapist to later continue in the form of video-call telerehabilitation. This means that the face-to-face relationship with the physiotherapist was achieved throughout the first month with presential pulmonary rehabilitation sessions, including an objective assessment, subjective exam, and motivational interviewing techniques. In the second month of the program, when telerehabilitation was set, it was not required to establish a new relationship with a remote unfamiliar professional: communication was remote, but the physiotherapist was the same and the program dynamics continued without the need for a reset.

Quality and security standards were requirements important to be guaranteed prior to the onset of telerehabilitation and included strategies such as the following: (1) confirmation of patient address and phone contacts; (2) alternative contact plan with a caregiver, familiar, neighbor, or friend; (3) printed tutorial of tablet usage during telerehabilitation; and (4) individual action-plan as proposed by the Living Well with COPD™ program.

It was essential to ensure the technical functionality requirements were met on the week prior to the start of telerehabilitation, with a group intervention in the hospital setting helpful to (1) ensure first contact with tablet and earphones and a handling demonstration; (2) ensure first usage of domiciliary equipment to be delivered and in-person repetition of proceedings for self-monitoring; (3) enable simulation of a remote session with each patient acting solo while communicating via a tablet with the physiotherapist; and (4) focus attention on systematic self-monitoring with a registered routine as a method.

Ensuring home environment appropriateness requirements were met necessitated a dynamic strategy to succeed with the installation at each patient's home scenario. For this purpose, the physiotherapist teamed up with the logistics and transportation staff, and all equipment was delivered in-person to the patient with a domiciliary visit, adjusting the appropriateness of the setting to match the requirements of the telerehabilitation sessions.

Finally, requirements of telesetting skills were very important as add-ons in clinical practice. At the hospital, the physiotherapist had to be exclusively dedicated to telerehabilitation, and video calls were operationalized as sequences and were not continuous. This strategy was fundamental to achieving good quality video images and sound communications, optimizing time management and effectiveness with real-time remote monitoring and simultaneous registration of patient clinical files. Hence, the patient was scheduled for a first video contact with only the physiotherapist alone, and afterward, the rest of the team were video connected and disconnected dynamically, enrolling two different patients at the same time, as a strategy to preserve group identity and peer reinforcement. All patients were successful in providing feedback and accomplishing the purpose of exercise training. None of the patients had experienced previous health interventions by video call, and only one of the patients had previously used a tablet.

Table 3 presents pulmonary telerehabilitation outcomes. The difference between median values was statistically significant in CAT scores from 15.5 to 10.5 (p = 0.004), surpassing the minimal clinically important difference of 2 points. Also, there was a statistically significant difference between medians of PRAISE score from 49.5 to 53.0 (p = 0.006) close to the minimal clinically important difference of 3.59. The objective assessment excluded six participants due to imposed COVID-19 pandemic constraints for face-to-face hospital evaluations as a protocol.

TABLE 3

Table 3. Pulmonary telerehabilitation outcomes.

When the pulmonary rehabilitation program concluded, patients reported a mean level of satisfaction with rehabilitation goals achievement scores of 88.1 ± 8.6% (range between 80 and 100%). Also, patients reported a mean level of satisfaction values with pulmonary rehabilitation with telerehabilitation experienced as a model of care of 95.4 ± 6.3% (range between 80 and 100%).

Discussion

The engagement of all stakeholders in the participatory research process, especially the patients, was a cornerstone for the success of telerehabilitation implementation. Such a methodological benefit has also been described in optimizing the implementation of pulmonary rehabilitation for COPD patients with limited accessibility due to geographical distances (45) and also in telerehabilitation redesigned for underserved Hispanic and African American patients with COPD (46).

It is important to acknowledge a core set of conceptual reasons for selecting telerehabilitation as an appropriate model of care to develop. As pulmonary rehabilitation is widely underutilized and frequently inaccessible to patients (47), current programs need to be upgraded on means of delivery to boost an effective waiting-list reduction. For this purpose, there has been a significant telemedicine contribution to modernizing healthcare within the framework of integrated care and the chronic care model of disease management (48). No less relevant is the fact that the provision of care needs to be redesigned to promote patient autonomy and self-efficacy (49), and telerehabilitation provides remote care to take place exactly where change needs to happen: in the patients' own living environments. All of these reasons prevail and became even more relevant, making telerehabilitation a new standard in a Post-COVID-19 world (50).

Altogether we have found five major groups of requirements for setting up pulmonary telerehabilitation: (1) pulmonary rehabilitation core principles, (2) quality and security standards, (3) technological functionality, (4) home environment appropriateness, and (5) telesetting skills. Such a framework led to the development of operational strategies aiming to empower patient self-efficacy with increased digital skills and health literacy, promote safety and quality conditions for real-time remote person-centered care, and optimize the efficiency of the exercise-based intervention with tech-enabled remote healthcare. We believe that such operational experience is an advantageous background to consider for those redesigning upgraded telerehabilitation programs.

A noteworthy remark is that the onset of this telerehabilitation model was supported by hospital services and human resources and required additional costs to the standard of care, including logistics, transport, and communications, as briefly described. This proof-of-concept research demonstrated the feasibility of telerehabilitation implementation in a setting before the COVID-19 pandemic. A further step was to prove beyond the clinical benefit a cost-benefit analysis of pulmonary rehabilitation standard-of-care vs. pulmonary telerehabilitation innovation by means of an economic study, which was beyond the scope of the present study. Interesting is that what used to be a struggle for investment, mainly regarding costly communication expenses, is nowadays a widespread area of funding with promising exponential development over the years to come.

This study describes an increase in patients' reported quality of life and perceived self-efficacy with telerehabilitation, a finding that requires future research with a larger sample to strengthen the evidence. An important outcome to emphasize was the high level of patient satisfaction not only about rehabilitation goals achievement but more importantly about pulmonary rehabilitation with telerehabilitation experienced. Such patient-reported outcomes and experiences support telerehabilitation as an emerging model of care with high acceptance from its end-users. With the COVID-19 pandemic, this was one of the many ongoing trials that suspended some or all research activities (51), as it was no exception to global rehabilitation services that experienced partial or complete disruption (52). Because of this, a major study limitation is the incomplete objective patient outcomes assessment, as face-to-face hospital evaluations as a protocol were no longer authorized due to the declared COVID-19 pandemic. Also, external validity may be limited, as there might be various frameworks within telerehabilitation developers, given possible multiple operational scenarios with different requirements for telerehabilitation setting up and implementation. This includes digital health literacy levels of both patients and healthcare professionals (53). Therefore, future research collecting global multicentric experiences of telerehabilitation implementation might be relevant to leverage an upgraded restart of the pulmonary rehabilitation study outside of the pandemic scenario.

Current worldwide developments have made pulmonary telerehabilitation rise rapidly from being a promising area of research (49, 54, 55) to a required shift to maintain ongoing pulmonary rehabilitation programs during the COVID-19 pandemic (52, 56, 57). This makes the reported operational experience resourceful to those who are engaged with telerehabilitation in the frontline, not as an add-on but instead as a necessary intervention. Naturally, emerging models will continue to evolve and produce increased diversity in pulmonary rehabilitation delivery of care (4), as nowadays telerehabilitation plays a major part in the solution to improve the effectiveness, accessibility, and resilience of healthcare systems worldwide.

Data Availability Statement

The original contributions presented in the study are included in the article/supplementary material, further inquiries can be directed to the corresponding author/s.

Ethics Statement

The studies involving human participants were reviewed and approved by Ethics Committee of Centro Hospitalar Universitário Lisboa Norte, and Centro Académico de Medicina de Lisboa (number 43/17). The patients/participants provided their written informed consent to participate in this study.

Author Contributions

CS: conceptualization, methodology, investigation, formal analysis, and writing–original draft. FR: conceptualization, investigation, and writing—review and editing. CC: writing—review and editing. CB: conceptualization and writing—review and editing. All authors edited the manuscript and approved the final draft.

Funding

This work was supported by Fundação para a Ciência e Tecnologia (FCT) and Nippon Gases Portugal under the Ph.D. studentship in Industry grant PDE/BDE/127785/2016 awarded to CS.

Conflict of Interest

CC is employed by Nippon Gases Portugal.

The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Publisher's Note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

Acknowledgments

Authors are grateful to everyone from Centro Hospitalar Universitário Lisboa Norte, E.P.E. who made telerehabilitation setting up and implementation possible: Carlos Martins, Teresa Magalhães, Ana Barardo, Daniel Ferro, Luis Pinheiro, Mónica Lopes dos Reis, Pedro Leite, Rui Leão, Nuno Jorge, António Macedo, Diogo Carvalho, Eduardo Carriço, Serafim Gomes, Gonçalo Rodrigues, Carla Baptista and Marta Miguéns. Authors are also thankful to Fundação Vodafone Portugal for providing mobile technology support to telerehabilitation activity, with a special appreciation to Ana Veríssimo and Mauro Gonçalves.

References

1. Peterson CB, Hamilton C, Hasvold P. From Innovation to Implementation: eHealth in the WHO European Region. Copenhagen: WHO Regional Office for Europe (2016).

Google Scholar

2. Spruit MA, Singh SJ, Garvey C, ZuWallack R, Nici L, Rochester C, et al. An official American Thoracic Society/European Respiratory Society statement: key concepts and advances in pulmonary rehabilitation. Am J Respir Crit Care Med. (2013) 188:e13–64. doi: 10.1164/rccm.201309-1634ST

PubMed Abstract | CrossRef Full Text | Google Scholar

3. Holland AE, Cox NS, Houchen-Wolloff L, Rochester CL, Garvey C, ZuWallack R, et al. Defining modern pulmonary rehabilitation. An official American Thoracic Society Workshop Report. Ann Am Thorac Soc. (2021) 18:e12–29. doi: 10.1513/AnnalsATS.202102-146ST

PubMed Abstract | CrossRef Full Text | Google Scholar

4. Hansen H, Nolan C. Emerging models. In: Hurst J, editor. Pulmonary Rehabilitation - ERS Monograph. 93. Norwich: European Respiratory Society (2021). p. 294–310. doi: 10.1183/2312508X.10019220

CrossRef Full Text | Google Scholar

5. Holland AE, Hill CJ, Rochford P, Fiore J, Berlowitz DJ, McDonald CF. Telerehabilitation for people with chronic obstructive pulmonary disease: feasibility of a simple, real time model of supervised exercise training. J Telemed Telecare. (2013) 19:222–6. doi: 10.1177/1357633x13487100

PubMed Abstract | CrossRef Full Text | Google Scholar

6. Bourne S, DeVos R, North M, Chauhan A, Green B, Brown T, et al. Online versus face-to-face pulmonary rehabilitation for patients with chronic obstructive pulmonary disease: randomised controlled trial. BMJ Open. (2017) 7:e014580. doi: 10.1136/bmjopen-2016-014580

PubMed Abstract | CrossRef Full Text | Google Scholar

7. Hansen H, Bieler T, Beyer N, Kallemose T, Wilcke JT, Østergaard LM, et al. Supervised pulmonary tele-rehabilitation versus pulmonary rehabilitation in severe COPD: a randomised multicentre trial. Thorax. (2020) 75:413–21. doi: 10.1136/thoraxjnl-2019-214246

PubMed Abstract | CrossRef Full Text | Google Scholar

8. Vasilopoulou M, Papaioannou AI, Kaltsakas G, Louvaris Z, Chynkiamis N, Spetsioti S, et al. Home-based maintenance tele-rehabilitation reduces the risk for acute exacerbations of COPD, hospitalisations and emergency department visits. Eur Respir J. (2017) 49:1602129. doi: 10.1183/13993003.02129-2016

PubMed Abstract | CrossRef Full Text | Google Scholar

9. Galdiz JB, Gómez A, Rodriguez D, Guell R, Cebollero P, Hueto J, et al. Telerehabilitation programme as a maintenance strategy for COPD patients: a 12-month randomized clinical trial. Arch Bronconeumol. (2020) 57:195–204. doi: 10.1016/j.arbres.2020.03.034

PubMed Abstract | CrossRef Full Text | Google Scholar

10. Cox NS, Dal Corso S, Hansen H, McDonald CF, Hill CJ, Zanaboni P, et al. Telerehabilitation for chronic respiratory disease. Cochrane Database Syst Rev. (2021) 1:CD013040. doi: 10.1002/14651858.CD013040.pub2

PubMed Abstract | CrossRef Full Text | Google Scholar

11. Bergold J, Thomas S. Participatory research methods: a methodological approach in motion. Forum Qual Soc Res. (2012) 13:31. doi: 10.17169/fqs-13.1.1801

CrossRef Full Text | Google Scholar

12. Asaba E, Suarez-Balcazar Y. Participatory research: a promising approach to promote meaningful engagement. Scand J Occup Ther. (2018) 25:309–12. doi: 10.1080/11038128.2018.1541224

PubMed Abstract | CrossRef Full Text | Google Scholar

13. Orkin AM, Gill PJ, Ghersi D, Campbell L, Sugarman J, Emsley R, et al. Guidelines for reporting trial protocols and completed trials modified due to the COVID-19 pandemic and other extenuating circumstances: the CONSERVE 2021 statement. JAMA. (2021) 326:257–65. doi: 10.1001/jama.2021.9941

PubMed Abstract | CrossRef Full Text | Google Scholar

14. Puente-Maestu L, Palange P, Casaburi R, Laveneziana P, Maltais F, Neder JA, et al. Use of exercise testing in the evaluation of interventional efficacy: an official ERS statement. Eur Respir J. (2016) 47:429–60. doi: 10.1183/13993003.00745-2015

PubMed Abstract | CrossRef Full Text | Google Scholar

15. Radtke T, Crook S, Kaltsakas G, Louvaris Z, Berton D, Urquhart DS, et al. ERS statement on standardisation of cardiopulmonary exercise testing in chronic lung diseases. Eur Respir Rev. (2019) 28:180101. doi: 10.1183/16000617.0101-2018

PubMed Abstract | CrossRef Full Text | Google Scholar

16. Wasserman K, Hansen J, Sue D, Casaburi R, Whipp B. Normal Values. Principles of Exercise Testing and Interpretation. 3rd ed. Baltimore, MD: Lippincott Williams & Wilkins (1999).

Google Scholar

17. Holland AE, Spruit MA, Singh SJ. How to carry out a field walking test in chronic respiratory disease. Breathe. (2015) 11:128–39. doi: 10.1183/20734735.021314

PubMed Abstract | CrossRef Full Text | Google Scholar

18. Holland AE, Spruit MA, Troosters T, Puhan MA, Pepin V, Saey D, et al. An official European Respiratory Society/American Thoracic Society technical standard: field walking tests in chronic respiratory disease. Eur Respir J. (2014) 44:1428–46. doi: 10.1183/09031936.00150314

PubMed Abstract | CrossRef Full Text | Google Scholar

19. Singh SJ, Puhan MA, Andrianopoulos V, Hernandes NA, Mitchell KE, Hill CJ, et al. An official systematic review of the European Respiratory Society/American Thoracic Society: measurement properties of field walking tests in chronic respiratory disease. Eur Respir J. (2014) 44:1447–78. doi: 10.1183/09031936.00150414

PubMed Abstract | CrossRef Full Text | Google Scholar

20. Bohannon RW, Crouch R. 1-Minute Sit-to-stand test: systematic review of procedures, performance, and clinimetric properties. J Cardiopulm Rehabil Prev. (2019) 39:2–8. doi: 10.1097/HCR.0000000000000336

PubMed Abstract | CrossRef Full Text | Google Scholar

21. Vaidya T, de Bisschop C, Beaumont M, Ouksel H, Jean V, Dessables F, et al. Is the 1-minute sit-to-stand test a good tool for the evaluation of the impact of pulmonary rehabilitation? Determination of the minimal important difference in COPD. Int J Chron Obstruct Pulmon Dis. (2016) 11:2609–16. doi: 10.2147/COPD.S115439

PubMed Abstract | CrossRef Full Text | Google Scholar

22. Furlanetto KC, Correia NS, Mesquita R, Morita AA, do Amaral DP, Mont'Alverne DGB, et al. Reference values for 7 different protocols of simple functional tests: a multicenter study. Arch Phys Med Rehabil. (2022) 103:20–8.e5. doi: 10.1016/j.apmr.2021.08.009

PubMed Abstract | CrossRef Full Text | Google Scholar

23. Skumlien S, Hagelund T, Bjørtuft O, Ryg MS. A field test of functional status as performance of activities of daily living in COPD patients. Respir Med. (2006) 100:316–23. doi: 10.1016/j.rmed.2005.04.022

PubMed Abstract | CrossRef Full Text | Google Scholar

24. Gulart AA, Munari AB, Klein SR, Santos da Silveira L, Mayer AF. The glittre-ADL test cut-off point to discriminate abnormal functional capacity in patients with COPD. COPD. (2018) 15:73–8. doi: 10.1080/15412555.2017.1369505

PubMed Abstract | CrossRef Full Text | Google Scholar

25. Gulart AA, Araujo CLP, Munari AB, Santos KD, Karloh M, Foscarini BG, et al. The minimal important difference for Glittre-ADL test in patients with chronic obstructive pulmonary disease. Braz J Phys Ther. (2020) 24:54–60. doi: 10.1016/j.bjpt.2018.11.009

PubMed Abstract | CrossRef Full Text | Google Scholar

26. Reis CMD, Karloh M, Fonseca FR, Biscaro RRM, Mazo GZ, Mayer AF. Functional capacity measurement: reference equations for the Glittre Activities of Daily Living test. J Bras Pneumol. (2018) 44:370–7. doi: 10.1590/s1806-37562017000000118

PubMed Abstract | CrossRef Full Text | Google Scholar

27. Robles PG, Mathur S, Janaudis-Fereira T, Dolmage TE, Goldstein RS, Brooks D. Measurement of peripheral muscle strength in individuals with chronic obstructive pulmonary disease: a systematic review. J Cardiopulm Rehabil Prev. (2011) 31:11–24. doi: 10.1097/HCR.0b013e3181ebf302

PubMed Abstract | CrossRef Full Text | Google Scholar

28. Holden M, Fyfe M, Poulin C, Bethune B, Church C, Hepburn P, et al. Handgrip strength in people with chronic obstructive pulmonary disease: a systematic review and meta-analysis. Phys Ther. (2021) 101:pzab057. doi: 10.1093/ptj/pzab057

PubMed Abstract | CrossRef Full Text | Google Scholar

29. Wang I, Bohannon RW, Kapellush J, Rahman MH, Liu CJ, Chang PF. Predicting the handgrip strength across the age span: Cross-validating reference equations from the 2011 NIH toolbox norming study. J Hand Ther. (2020) 35:131–41. doi: 10.1016/j.apmr.2020.09.171

PubMed Abstract | CrossRef Full Text | Google Scholar

30. Ringbaek T, Brøndum E, Martinez G, Lange P. EuroQoL in assessment of the effect of pulmonary rehabilitation COPD patients. Respir Med. (2008) 102:1563–7. doi: 10.1016/j.rmed.2008.06.016

PubMed Abstract | CrossRef Full Text | Google Scholar

31. Zanini A, Aiello M, Adamo D, Casale S, Cherubino F, Della Patrona S, et al. Estimation of minimal clinically important difference in EQ-5D visual analog scale score after pulmonary rehabilitation in subjects with COPD. Respir Care. (2015) 60:88–95. doi: 10.4187/respcare.03272

PubMed Abstract | CrossRef Full Text | Google Scholar

32. Jones PW, Harding G, Berry P, Wiklund I, Chen WH, Kline Leidy N. Development and first validation of the COPD Assessment Test. Eur Respir J. (2009) 34:648–54. doi: 10.1183/09031936.00102509

PubMed Abstract | CrossRef Full Text | Google Scholar

33. Dodd JW, Hogg L, Nolan J, Jefford H, Grant A, Lord VM, et al. The COPD assessment test (CAT): response to pulmonary rehabilitation. A multicentre, prospective study. Thorax. (2011) 66:425–9. doi: 10.1136/thx.2010.156372

PubMed Abstract | CrossRef Full Text | Google Scholar

34. Mahler DA, Wells CK. Evaluation of clinical methods for rating dyspnea. Chest. (1988) 93:580–6. doi: 10.1378/chest.93.3.580

PubMed Abstract | CrossRef Full Text | Google Scholar

35. Garrod R, Bestall JC, Paul EA, Wedzicha JA, Jones PW. Development and validation of a standardized measure of activity of daily living in patients with severe COPD: the London Chest Activity of Daily Living scale (LCADL). Respir Med. (2000) 94:589–96. doi: 10.1053/rmed.2000.0786

PubMed Abstract | CrossRef Full Text | Google Scholar

36. Pitta F, Probst VS, Kovelis D, Segretti NO, Mt Leoni A, Garrod R, et al. [Validation of the Portuguese version of the London Chest Activity of Daily Living Scale (LCADL) in chronic obstructive pulmonary disease patients]. Rev Port Pneumol. (2008) 14:27–47. doi: 10.1016/S2173-5115(09)70242-8

CrossRef Full Text | Google Scholar

37. Puhan MA, Frey M, Büchi S, Schünemann HJ. The minimal important difference of the hospital anxiety and depression scale in patients with chronic obstructive pulmonary disease. Health Qual Life Outcomes. (2008) 6:46. doi: 10.1186/1477-7525-6-46

PubMed Abstract | CrossRef Full Text | Google Scholar

38. Vincent E, Sewell L, Wagg K, Deacon S, Williams J, Singh S. Measuring a change in self-efficacy following pulmonary rehabilitation: an evaluation of the PRAISE tool. Chest. (2011) 140:1534–9. doi: 10.1378/chest.10-2649

PubMed Abstract | CrossRef Full Text | Google Scholar

39. Santos CD, Santos AJ, Santos M, Rodrigues F, Bárbara C. Pulmonary rehabilitation adapted index of self-efficacy (PRAISE) validated to Portuguese respiratory patients. Pulmonology. (2019) 25:334–9. doi: 10.1016/j.pulmoe.2019.06.003

PubMed Abstract | CrossRef Full Text | Google Scholar

40. Nasreddine ZS, Phillips NA, Bédirian V, Charbonneau S, Whitehead V, Collin I, et al. The Montreal Cognitive Assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc. (2005) 53:695–9. doi: 10.1111/j.1532-5415.2005.53221.x

PubMed Abstract | CrossRef Full Text | Google Scholar

41. Pierobon A, Ranzini L, Torlaschi V, Sini Bottelli E, Giardini A, Bruschi C, et al. Screening for neuropsychological impairment in COPD patients undergoing rehabilitation. PLoS ONE. (2018) 13:e0199736. doi: 10.1371/journal.pone.0199736

PubMed Abstract | CrossRef Full Text | Google Scholar

42. Strassmann A, Guler M, Steurer-Stey C, Lana KD, Carron T, Braun J, et al. Nationwide implementation of the self-management program “Living well with COPD”: Process and effectiveness evaluation using a mixed-methods approach. Patient Educ Couns. (2021) 105:670–8. doi: 10.1016/j.pec.2021.06.018

PubMed Abstract | CrossRef Full Text | Google Scholar

43. Santos C, Rodrigues F, Santos J, Morais L, Bárbara C. Pulmonary rehabilitation in COPD: effect of 2 aerobic exercise intensities on subject-centered outcomes–a randomized controlled trial. Respir Care. (2015) 60:1603–9. doi: 10.4187/respcare.03663

PubMed Abstract | CrossRef Full Text | Google Scholar

44. Damschroder LJ, Aron DC, Keith RE, Kirsh SR, Alexander JA, Lowery JC. Fostering implementation of health services research findings into practice: a consolidated framework for advancing implementation science. Implement Sci. (2009) 4:50. doi: 10.1186/1748-5908-4-50

PubMed Abstract | CrossRef Full Text | Google Scholar

45. Hug S, Cavalheri V, Gucciardi DF, Norman R, Hill K. OPTImising the implementation of pulMonary rehAbiLitation in people with chronic obstructive pulmonary disease (the OPTIMAL study): mixed methods study protocol. BMC Pulm Med. (2020) 20:286. doi: 10.1186/s12890-020-01322-4

PubMed Abstract | CrossRef Full Text | Google Scholar

46. Pekmezaris R, Kozikowski A, Pascarelli B, Wolf-Klein G, Boye-Codjoe E, Jacome S, et al. A telehealth-delivered pulmonary rehabilitation intervention in underserved hispanic and African American patients with chronic obstructive pulmonary disease: a community-based participatory research approach. JMIR Form Res. (2020) 4:e13197. doi: 10.2196/13197

PubMed Abstract | CrossRef Full Text | Google Scholar

47. Rochester CL, Vogiatzis I, Holland AE, Lareau SC, Marciniuk DD, Puhan MA, et al. An official American Thoracic Society/European Respiratory Society Policy statement: enhancing implementation, use, and delivery of pulmonary rehabilitation. Am J Respir Crit Care Med. (2015) 192:1373–86. doi: 10.1164/rccm.201510-1966ST

PubMed Abstract | CrossRef Full Text | Google Scholar

48. Donner CF, ZuWallack R, Nici L. The role of telemedicine in extending and enhancing medical management of the patient with chronic obstructive pulmonary disease. Medicina. (2021) 57:726. doi: 10.3390/medicina57070726

PubMed Abstract | CrossRef Full Text | Google Scholar

49. Selzler AM, Wald J, Sedeno M, Jourdain T, Janaudis-Ferreira T, Goldstein R, et al. Telehealth pulmonary rehabilitation: a review of the literature and an example of a nationwide initiative to improve the accessibility of pulmonary rehabilitation. Chron Respir Dis. (2018) 15:41–7. doi: 10.1177/1479972317724570

PubMed Abstract | CrossRef Full Text | Google Scholar

50. Tsutsui M, Gerayeli F, Sin DD. Pulmonary rehabilitation in a Post-COVID-19 world: telerehabilitation as a new standard in patients with COPD. Int J Chron Obstruct Pulmon Dis. (2021) 16:379–91. doi: 10.2147/COPD.S263031

PubMed Abstract | CrossRef Full Text | Google Scholar

51. Mitchell EJ, Ahmed K, Breeman S, Cotton S, Constable L, Ferry G, et al. It is unprecedented: trial management during the COVID-19 pandemic and beyond. Trials. (2020) 21:784. doi: 10.1186/s13063-020-04711-6

PubMed Abstract | CrossRef Full Text | Google Scholar

52. Sebio-García R. Pulmonary rehabilitation: time for an upgrade. J Clin Med. (2020) 9:2742. doi: 10.3390/jcm9092742

PubMed Abstract | CrossRef Full Text | Google Scholar

53. Conard S. Best practices in digital health literacy. Int J Cardiol. (2019) 292:277–9. doi: 10.1016/j.ijcard.2019.05.070

PubMed Abstract | CrossRef Full Text | Google Scholar

54. Marquis N, Larivée P, Saey D, Dubois MF, Tousignant M. In-home pulmonary telerehabilitation for patients with chronic obstructive pulmonary disease: a pre-experimental study on effectiveness, satisfaction, and adherence. Telemed J eHealth. (2015) 21:870–9. doi: 10.1089/tmj.2014.0198

PubMed Abstract | CrossRef Full Text | Google Scholar

55. Cox NS, McDonald CF, Alison JA, Mahal A, Wootton R, Hill CJ, et al. Telerehabilitation versus traditional centre-based pulmonary rehabilitation for people with chronic respiratory disease: protocol for a randomised controlled trial. BMC Pulm Med. (2018) 18:71. doi: 10.1186/s12890-018-0646-0

PubMed Abstract | CrossRef Full Text | Google Scholar

56. Jácome C, Marques A, Oliveira A, Rodrigues LV, Sanches I. Pulmonary telerehabilitation: an international call for action. Pulmonology. (2020) 26:335–7. doi: 10.1016/j.pulmoe.2020.05.018

PubMed Abstract | CrossRef Full Text | Google Scholar

57. Houchen-Wolloff L, Steiner MC. Pulmonary rehabilitation at a time of social distancing: prime time for tele-rehabilitation? Thorax. (2020) 75:446–7. doi: 10.1136/thoraxjnl-2020-214788

PubMed Abstract | CrossRef Full Text | Google Scholar