Volume 22, Issue 1 (March 2024)                   Iranian Rehabilitation Journal 2024, 22(1): 15-24 | Back to browse issues page


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Nazir A, Tiksnadi B B, Ridzki M F F A. Exercise-based Rehabilitation to Improve Exercise Tolerance of Severe COVID-19 Survivors: A Review Paper. Iranian Rehabilitation Journal 2024; 22 (1) :15-24
URL: http://irj.uswr.ac.ir/article-1-1630-en.html
1- Department of Physical Medicine and Rehabilitation, Faculty of Medicine, Dr. Hasan Sadikin General Hospital, Padjadjaran University, Bandung, Indonesia.
2- Department of Cardiology and Vascular Medicine, Faculty of Medicine, Dr. Hasan Sadikin General Hospital, Padjadjaran University, Bandung, Indonesia.
3- Faculty of Medicine, Padjadjaran University, Bandung, Indonesia.
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Introduction
Muscle weakness after acute phase recovery from COVID-19 is a real problem that could be experienced by survivors. As many as 10%-20% of COVID-19 patients experience persistent symptoms weeks to months after the acute phase of COVID-19 [1]. Research shows that survivors of severe COVID-19 can have various functional complications as a “follow-up”, such as persistent shortness of breath and post-intensive care syndrome which is characterized by muscle weakness, joint stiffness, deconditioning, cognitive dysfunction, psychiatric illness, and quadriparesis that persist after resolution of the acute illness [2–4].
COVID-19 survivors may experience a decrease in long-term exercise tolerance [5]. Research showed that COVID-19 survivors can experience a decrease in exercise capacity (VO2 max). VO2 max decreased by more than 10% compared to before infection [6]. Other studies showed that survivors of COVID-19 could have a VO2 max <80% of the predicted value after 3 months of being discharged from the hospital. The distance of the six-minute walk test (6-MWT) was decreased and a minimum SpO2 value in the 6-MWT was <96% 6 months after discharge from the hospital [7, 8]. The decrease in the functional capacity of COVID-19 survivors is not only caused by pulmonary organ dysfunction and decreased gas exchange but also by extrapulmonary factors such as cardiac dysfunction and muscle weakness associated with long-term hospitalization and immobilization after recovery from the acute phase of COVID-19 [9, 10]. Survivors of severe COVID-19 could have a significantly greater decrease in exercise tolerance than survivors of mild COVID-19 [11-13]. Decreased exercise tolerance in COVID-19 survivors can result in increased morbidity and mortality, decreased quality of life, and a continuous increase in the burden on the health system [10, 14].
Rehabilitation is a multidisciplinary intervention that reduces morbidity, increases functional independence, and improves the ability to carry out daily activities. Based on the characteristics and complications caused by COVID-19, exercise-based multidisciplinary rehabilitation has the opportunity to increase functional capacity, provide a better prognosis, prevent long-term disability, and improve the quality of life of COVID-19 survivors [11, 15–17].
The magnitude of the negative physical impact on the survivors of COVID-19 and the absence of standardized guidelines in the implementation of rehabilitation were the reasons to conduct this review. In addition, the presence of potential barriers is important to know to determine the strategy to overcome the rehabilitation problems. This review aimed to determine the form, results, and barriers to exercise-based rehabilitation programs for severe COVID-19 survivors.

Materials and Methods
This study uses an article review method by collecting and synthesizing data from the article related to exercise-based rehabilitation in severe COVID-19 survivors. Searching for the article was carried out from August to October 2021. We used the PubMed database as a search media with the keywords ([‘COVID-19’ OR ‘COVID-19’ OR ‘SARS CoV-2’ OR ‘post COVID-19’]AND [‘rehabilitation’]). The type of articles used were original articles and case reports published in the last 2 years (2019-2021), available in English, and accessible in PDF or HTML format. Articles were excluded if they did not fit the research topic and were not available in full text. The article search flow is described in Figure 1.



Results
There were a total of 4691 articles found at the initial screening using keywords. In the next screening using the inclusion and exclusion criteria and after reading the whole articles, we found 9 articles that matched the topic. Of these, 7 articles were original articles and 2 case reports (Figure 1). Nine articles discussed the forms and outcomes of exercise-based rehabilitation and no article discussed the barriers to rehabilitation. Nine articles outlined cardiopulmonary rehabilitation as a rehabilitation effort for COVID-19 survivors which consisted of a combination of various exercises such as aerobic exercise, resistance training, strength training, activities of daily living (ADL) training, and breathing exercises. A total of 9 articles explained an increase in functional ability and quality of life of COVID-19 survivors in severe cases (Table 1) [2,15,18-24]. 





Discussion
Rehabilitation of COVID-19 survivors focuses on treating ongoing disorders including impaired mobility, respiratory function, nutrition, and communication to promote independence in performing ADL. The rehabilitation program provided is an ongoing treatment that is specific in nature according to the needs and abilities of the patient [12, 25].

Exercise-based rehabilitation for severe COVID-19 survivors 
Based on the articles reviewed, it was found that the exercise to increase exercise tolerance in survivors of severe COVID-19 cases was generally given in the form of physical exercise which was included in the cardiopulmonary rehabilitation program [15, 18, 23, 24]. The physical exercise program consisted of aerobic exercise, muscle strength training (weight training), resistance training, breathing exercises, and ROM exercises. The exercise program was given since the patient was hospitalized until the outpatient phase [18–20]. These forms of exercise are also supported by several previous studies discussing rehabilitation in COVID-19 survivors. 
Gentil et al. (2021) recommended resistance training for COVID-19 survivors. The form of resistance training was resistance exercise with a low-volume and multi-joint. In addition, low external load resistance training can also be carried out by the patient and can provide the same results as high external load resistance training which is carried out with greater effort. As an alternative, high-velocity resistance training can be given if the patient cannot perform low/high external load training. [26].
A review article conducted by Agostini et al. (2021) mentioned the recommendation of aerobic exercise starting with low to moderate-intensity exercise which was increased gradually according to individual abilities [27]. Another review article study was conducted by Calabrese et al. (2021) recommended interval aerobic training with moderate to high intensity performed 3-5 times a week, for COVID-19 survivors [17].
Individually prescribed exercises according to the ability of the patient could also be given [18, 28]. The rehabilitation program can be provided for a minimum of 3 weeks in the inpatient phase and for 3 weeks during the outpatient phase [2]. Home-based exercise with telerehabilitation can also be given as a substitution for face-to-face rehabilitation programs [17]. There is no standard protocol for physical exercise for COVID-19 survivors with severe cases yet, either in the inpatient or outpatient phase.

Result of exercise-based rehabilitation for COVID-19 survivors
The exercise-based cardiopulmonary rehabilitation program given to severe COVID-19 survivors could improve exercise tolerance, functional independence in ADL, as well as general health status which has a positive impact on the quality of life of survivors [2, 15, 18–20, 22–24]. A cohort study conducted by Olezene et al. (2021) showed that the multimodal rehabilitation program given to survivors of severe COVID-19 cases increased exercise tolerance as measured by an increase in the 6-MWT distance of 557.9 meters compared to before rehabilitation. This study also mentions an increase in 10-MWT speed of 0.61 meters/second and functional independence as measured by the ability for independence transfer and ambulation [2].
Another review reported similar results in an increase in 6-MWT distance and functional independence as measured by functional independence measure (FIM) after being given a combination of aerobic, endurance, strength, and breathing exercises [19, 20, 22, 24]. A rehabilitation program consisting of the series of these exercises which was increased gradually in intensity could also improve muscle strength and function as measured by an increase in bilateral hand muscle strength by 5 kg, peak quadriceps muscle strength by 21.2% of predicted value, and sit to stand speed by 3 seconds [15].
Articles reviewed in this study also described similar results with several previous studies. Agostini, et al. (2021) found that comprehensive cardiopulmonary rehabilitation improved mobilization and ADL functions as well as neuropsychological status [15, 21, 27]. A previous article review conducted by Gentil et al. (2021) found that resistance exercise could also improve cardiovascular function, physical ability, and functional capacity in addition to increased muscle mass strength [26]. 
A cohort study conducted by Puchner et al. (2021) also found an increase in lung capacity in COVID-19 survivors after multidisciplinary rehabilitation with a duration of 3 weeks [21]. In addition, cardiovascular rehabilitation consisting of aerobic and interval training had a positive impact on improving cardiovascular function, decreasing blood pressure after exercise, and respiratory function [17].
The barrier of exercise-based rehabilitation for COVID-19 survivors
There was no article found that discussed barriers to the rehabilitation of COVID-19 survivors. The scoping review by Wasilewski et al. (2021) [25] described barriers to COVID-19 rehabilitation which were divided as follows: 1) COVID-19 infectivity (causing limitation of patients’ access to rehabilitation facilities, prohibition to mobilize to public areas, prohibition to the involvement of the families in patients’ care, and closure of healthcare facilities); 2) Patient health status (diversity in the severity of COVID-19, disability, and instability of the patient’s condition); 3) Lack of guidance in the rehabilitation management; 4) Problems related to the availability of personal protective equipment; 5) Problems related to healthcare staff (decreased health status of medical personnel, high workload, and fear of being infected with COVID -19); and 6) Problems in the health system (lack of communication between levels, lack of costs, and unpreparedness of health services to provide rehabilitation services) [25]. Barriers to the rehabilitation of COVID-19 survivors can occur in all phases of care [29].
To our knowledge, this study is the first to specifically discuss exercises to increase exercise tolerance in COVID patients and this study explores exercises to increase exercise tolerance from inpatient care to outpatient care. So, the results of this study can be used as a basis for efforts to prevent lowering exercise tolerance in COVID patients by providing exercise as early as possible after the patient is admitted. The weakness of this study is searching only 1 search engine so there is the possibility of other similar studies that are not explored.

Conclusion 
Research on the rehabilitation of COVID-19 survivors is still limited in number, especially regarding the rehabilitation of severe cases survivors. Based on the reviewed articles, we found that the rehabilitation program was generally provided in both inpatient and outpatient cardiopulmonary rehabilitation programs. Exercises given were aerobic exercise, resistance, and strength training, as well as ADL, range of motion (ROM), breathing, and other exercises. The exercise program was given as needed and tailored to the patient’s needs. Exercise-based rehabilitation of severe COVID-19 survivors improved exercise tolerance, functional ability, and quality of life. Exercise could also improve organ function affected in the acute phase of COVID-19. There were several barriers encountered in the implementation of exercise-based rehabilitation such as the patient’s condition, COVID-19 infectivity, lack of guidelines, and issues related to the provision of health services. 

Ethical Considerations

Compliance with ethical guidelines

This systematic review is regarded exclusively on published literature. 

Funding
This research did not receive any grant from funding agencies in the public, commercial, or non-profit sectors

Authors' contributions
Conceptualization: Arnengsih Nazir; Supervision: Arnengsih Nazir and Badai Bhatara Tiksnadi; Methodology, investigation, writing, funding acquisition and resources: All authors.

Conflict of interest
The authors declared no conflict of interest

Acknowledgments
The author would like to thank Padjadjaran University and Dr. Hasan Sadikin General Hospital for the opportunity to conduct this work and for database facilitation.





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Article type: Reviews | Subject: Physical Medicine and Rehabilitation
Received: 2022/03/14 | Accepted: 2023/10/11 | Published: 2024/03/1

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