Rehabilitation Management to Improve Respiratory Function in Severe and Critical COVID-19 Survivors: A Literature Review

Post-acute COVID-19 symptoms impact the quality of life, and pulmonary rehabilitation is recommended. This study explored the implementation, outcomes, and barriers of such programs for severe and critical COVID-19 survivors, focusing on improving respiratory function. Articles search was conducted from October to November 2021 through Google Scholar and PubMed databases. Pulmonary rehabilitation programs in severe and critical cases of COVID-19 survivors have a similar purpose in other respiratory cases. Pulmonary rehabilitation programs, including breathing, resistance, stretching, cardiorespiratory endurance exercises, respiratory physiotherapy, relaxation techniques, and education, significantly improved lung function and reduced symptoms. No studies exploring barriers to pulmonary rehabilitation were found. In conclusion, pulmonary rehabilitation programs for COVID-19 survivors with severe and critical cases have improved respiratory functions.


Introduction
Coronavirus disease 2019 (COVID-19) is a global health issue with clinical manifestations that can develop into severe, critical, or even death, especially for older individuals and those with comorbidities. 1,2 COVID-19 survivors often experience post-acute COVID-19, which can be classified into subacute (symptoms persisting for 4-12 weeks) and chronic (persisting for more than 12 weeks). 3,4 Common symptoms include shortness of breath and fatigue, affecting various organ systems. 4,5 Post-acute COVID-19 is attributed to multiple factors, including the invasion of severe acute respiratory syn drome coronavirus 2 (SARS-CoV-2), leading to pulmo nary fibrosis and reduced lung function. 4,[6][7][8] Microvas cular thrombosis, the immune system-induced tissue damage, inflammation, and cytokine storm con tri bute to organ dysfunction and complications. 4,6,7,9 Pulmonary rehabilitation (PR) is recommended for severe and critical COVID-19 survivors to improve respiratory function and quality of life (QoL). The PR programs with exercise as one of the core components are administered to relieve symptoms, restore functional abilities, and reduce disability in order to improve overall QoL. 4,10 This was the first review to specifically explore pulmonary rehabilitation in managing respiratory function disorders in severe and critical COVID-19 cases. The potential benefits of PR in improving respiratory function and QoL for severe and critical COVID-19 survivors were highlighted. This study explored PR im plementation, outcomes, and barriers, providing insights for health professionals and policymakers in managing longterm COVID-19 effects and emphasizing com pre hensive care for post-acute patients.
or HTML format. The articles were initially selected based on their titles, abstracts, and keywords. After reading the whole text, data were displayed as text and table.

Results
Eight articles discussing the implementation and outcomes of PR were found and no articles discussing barriers. The literature search flow based on preferred reporting items for systematic reviews and meta-analyses is shown in Figure 1, and the summary of PR interventions and outcomes is shown in Table 1.

Implementation of Pulmonary Rehabilitation
COVID-19 survivors often experience residual symptoms even though they have been cured. 3,4 The PR program can be prescribed for COVID-19 survivors, especially in severe and critical cases, to relieve symptoms, improve quality of life, improve respiratory muscle function, and relieve symptoms of anxiety and depression. 13 The PR program for COVID-19 survivors includes breathing exercises, strength and stretching exer cises, cardiorespiratory endurance exercises, res pi rat ory physiotherapy, and relaxation technique. [11][12][13][14][15][16][17][18] Other interventions are psychological support, psycho therapy, nutri tional counseling, occupational therapy, and activity of daily living exercises in cali s thenics, speech therapy, and swallowing. 12,13,[16][17][18] One article recommends mobi li zation, such as free and paced walking, balance, and aerobic exercise. 15 Breathing exercises need to be carried out for COVID-19 survivors, especially in severe and critical cases, because lung function decreases in response to a cytokine storm in the acute phase. Decreased lung function is caused by impaired lung expansion due to alveolar damage to pulmonary fibrosis. 7,8 The intensive care unit care is involved in critical cases that cause the patient to experience muscle weakness related to mechanic al ventilation, which significantly accelerates and exacerbates respiratory muscle dysfunction. 4 Sun, et al., 13 applied the breathing method as the core of PR by adopting the 3-5-6 breathing method, three seconds of deep inspiration, then holding breath for three Table 1

Author (s) Year Study Design Rehabilitation Management Outcome
Liu, et al. 11 2020 Randomized controlled trial PR consisted of respiratory muscle, cough, Significant improvement in lung function (FEV1, diaphragm, stretching, and home exercises. FVC, FEV1/FVC, and DLCO) in the intervention group. Gloeckl, et al. 12 2021 A prospective, observational Comprehensive PR, including medical diagnos-1. Significant lung function improvement in a cohort study tics and treatment, resistance training, strength group of mild/moderate COVID-19 and severe training, patient education, respiratory physio-or critical. therapy, activity of daily living exercises, relax-2. Dyspnea, fatigue, and cough persist after ation techniques, occupational therapy, psycho-completing PR in severe/critical COVID-19. logical support, and nutritional counseling, is carried out for three weeks. Sun, et al. 13 2021 Before-after self-control pros-Breathing method exercises, respiratory muscle Dyspnea decreased, oxygen intake decreased, pective clinical trial training, stretching exercises, and psychotherapy. and oxygen saturation increased after 2-and 3-week PR. Shan, et al. 14 2020 Case report PR focusing on increasing activity tolerance and Improvement in oxygen saturation during excerendurance was performed for 10 days.
cise tests and incentive spirometer volume after PR. Spielmanns, et al. 15   to five seconds and slowly exhaling for six seconds. This exercise can be performed in a lying or standing position and is performed for three to four breath cycles per set with 30-60 seconds of rest, depending on the symptoms of shortness of breath. 13 Zhao, et al., mentioned that breathing exercises include posture management, breathing rhythm adjustment, thoracic expansion exercises, respiratory muscle mobilization, etc. 19 Several articles also recommend respiratory muscle training as a component of PR. 11,13,17,18,20 Respiratory muscle exercises, especially inspiratory muscles, can be performed in patients with inspiratory muscle weakness and can be performed with a frequency of up to two times a day. 13,17 Respiratory muscle exercises are carried out by inhalation and exhalation slowly to make the thorax expand, using diaphragmatic breathing and mobilization of the respiratory muscles for 15 minutes each in the right and left lateral decubitus positions alternately and followed by a supination position with a bridge exercise, alternating straight leg, air pedal, and ankle pump. 13,20 These exercises can also be performed using a commercial hand-held resistance device with ten breaths per set and performed in three sets using a positive expiratory pressure device if necessary. 11, 20 Liu, et al., stated that diaphragmatic exercises are performed with 30 maximal voluntary contractions of the diaphragm plus a 1-3 kg load on the anterior abdominal wall. 11 Based on the articles that discussed respiratory muscle training in COVID-19 survivors, no standard exercise has been found. 11,13,[16][17][18][19][20] Almost all the literature found includes strength training or limb resistance exercise as a PR component. 12,15-21 Strength training is performed using a strength training machine for approximately 30-60 minutes per session and five days a week. The resistance training includes butterfly forward/backward, rowing, back extension, abdominal trainer, weight training using machines, free weights, elastic resistance bands, latissimus pull, cable pull, and robotic arm training. 12,17,18,20,21 Neuromuscular electrical stimulation can be used to help strengthen muscles. 21 Patients undergo one to three sets of each exercise with 8-12 repetitions per set and two minutes of rest between sets with increasing intensity. 12,17, 19 Spielmanns, et al., declared that gymnastics can improve strength, endurance, coordination, range of motion, and balance. 15 Leg muscle strength training in COVID-19 survivors is carried out because of the cytokine storm in the acute phase of COVID-19, which causes damage to various organs, such as the dysfunction of skeletal muscles in the extremities, 7 which can worsen secondary to inactivity and immobilization. 4 The symptoms of fatigue and shortness of breath in COVID-19 survivors can cause survivors to limit their activi ties. 4,5 Stretching exercises are also recommended in PR, which consist of exercises in the upper and lower extremi ties that aim to improve muscle function, especial ly joint flexibility, the lack of which can prevent activities. Stretching exercises can also be combined with strength training in upper and lower extremity functional activities, including upward lift, lateral lift, abduction, chest enlargement and grasping, lifting, kicking, tip toeing, and stepping. 11,13 Fatigue and shortness of breath are the most common complaints found in COVID-19 survivors. 4,5 These symptoms are caused by damage to various organs that lead to a decrease in cardiorespiratory fitness. 22 Based on this review, it was found that cardiorespiratory endurance exercises are a major PR component. Endur ance training can be done by cycling at varying times, ranging from 10 to 60 minutes per session, and perform ed five to six times weekly. 12,15,17,18 Gloeckl, et al., discuss that exercise occurs at 60-70% of the peak work rate. 12 While, Puchner, et al., stated that endurance training is performed based on the cardiopulmonary exercise test at 50% of the highest pressure sustained for one second. 18 The intensity of each exercise can change depending on oxygen saturation and pulse rate. Oxygen administration may be performed if indicated. 17 Respiratory physiotherapy may vary from individual to individual. Physiotherapy is done twice to four times weekly for 30 minutes each session. 12 The techniques used in this physiotherapy include coughing techniques, mucus clearing, connective tissue massage, energy conser vation techniques, learning about breathing (pursed lip breathing, secretion mobilization, and dia phrag matic breathing), mucolytic inhalation therapy, etc. 12,15,17 Liu,et al., applied three sets of coughing exercises with 10 active coughs per set which can be done at home. 11 Many psychiatric changes occur in COVID-19 survivors, such as post-traumatic stress disorder, depress ion, and anxiety. 23 Relaxation techniques can be included as a component of rehabilitation to reduce anxiety levels in COVID-19 survivors. 24 Gloeckl, et al., 12 Spielmanns, et al., 15 and Büsching, et al., 16 also included relaxation techniques as part of PR. The relax at ion technique is carried out by progressive muscle relax at ion (Jacobson's technique) twice per week for 30 minutes. 12,15,16 Education as part of PR includes explanations about COVID-19 and general topics such as physical activity, oxygen therapy, and smoking cessation. 12 There was also an explanation about PR's importance in increas ing patient compliance in under going rehabilitation. 16 This education can be done by direct exposure or using booklets and videos. 12,17,19

Outcomes of Pulmonary Rehabilitation
The PR has been shown to improve lung function and symptoms of dyspnea in severe and critical COVID-19 survivors. [11][12][13][14][15][16][17][18] Liu, et al., showed significant improvement in lung function, including FEV1, FVC, FEV1/FVC, and DLCO in the intervention group. 11 These results were consistent with Hayden, et al., and Puchner, et al., which showed a significant increase in vital capacity, FVC, TLC, FEV1, DLCO, and PImax after PR. 17,18 PR has also improved the partial pressure of oxygen, incentive spirometry volume, and decreased the need for oxygen support. 14,15,17 However, the persistence of dyspnea and fatigue after they underwent PR was found in many survivors. 12 In addition, some symptoms, including exertional dyspnea, cough, fatigue, and phlegm production, also decreased. 13,17 Respiratory muscle exercise has in creased diaphragmatic strength and endurance in COVID-19 survivors due to increased PImax. 17 Strength and endurance of the diaphragm and other respiratory muscles are associated with increased lung function. 11 Breathing exercises can also improve lung compliance and volume, which increases ventilation and gas ex change and further causes an increase in tidal volume, diaphragm capacity, and lung compliance. 13 Controlled breathing patterns and holding breath for a certain time decreased hypoxemia and local atelectasis. 13 Improvement in symptoms is also caused by increased exercise capacity, exercise tolerance, and local muscle endurance as a result of a comprehensive PR program, as well as aerobic and resistance exercise. 11 Gloeckl,et al.,12 discussing resistance exercise as part of PR showed a significant improvement in lung function (FEV1 and FVC) in severe and critical post-acute COVID-19 patients.

Barrier to Pulmonary Rehabilitation
No studies exploring barriers to pulmonary rehabilitation in COVID-19 survivors were found. Only one review by Wasilewski, et al., 25 discussed barriers to PR, including COVID-19 infectivity, the varied health status of patients, lack of literature, insufficient PPE, problems related to rehabilitation staff, and health system issues. The varying degrees of severity of COVID-19 patients can be challenging in prescribing and initiating rehabilitat ion. Disability and the unstable condition of the patient can also become obstacles. 25 Korupolu, et al., showed that the patient's ability to care for themselves and the caregiver's availability were inhibiting factors for rehabilitation in the outpatient unit. 21 The high number of COVID-19 cases and limited PPE and staff are also obstacles to rehabilitation. 21, 25 Wasilewski, et al., 25 also mentioned that the problems of the rehabilitation staff, such as high workloads, declining staff health, and fear of being infected with COVID-19, could prove obstacles. The infectivity of COVID-19 is also one of the considerations in the implementation of the rehabilitation program. 21,25 Limited access to rehabi li tation due to isolation procedures and the closure of rehabilitation centers has also occurred due to the increase in COVID-19, so the treatment focuses on the respiratory management of COVID-19 only. 25,26 Conversely, it is also difficult to implement the rehabilitation program to implement physical distancing. Families should also not be involved in the care of COVID-19 patients. 25 The health system issue is a challenge for implementing the rehabilitation program. Lack of coordi nation at all health system levels limits rehabilitation implementation's effectiveness. Lack of funding to support telerehabilitation and other infrastructure, as well as very strict billing procedures that reduce the time and quality of patient care, also hinder the rehabilitation program implementation. 25 This review specifically discussed the implement at ion, outcomes, and barriers of PR, even though the collected data were limited. This review can be used as a reference to explore more about this topic. However, there were some limitations, such as a limited database (only PubMed and Google Scholar), only written in English, and a short search period, so there are possible different outcomes if the review was done using more databases, not limited to English, and longer searching period. Future studies can be done by correct ing these.

Conclusion
The PR program in severe and critical cases of COVID-19 survivors aims to improve the QoL by alleviat ing symptoms, restoring functional abilities, and reducing disability. The PR program includes breathing, strength, stretching, cardiorespiratory endurance exercises, respiratory physiotherapy, relaxation tech niques, and education. Some articles stated that PR signi ficantly improves lung function and reduces the symp toms.

Ethics Approval and Consent to Participate
Not applicable. ance or presentation of the work described in this manuscript.

Availability of Data and Materials
The data used in this study were publicly available in the Google Scholar and PubMed databases.

Authors' Contribution
AN contributed to the conception and design of the study. AN, RN, and SAW drafted the article or revised it critically for important intellectual content and final approval of the version to be submitted.