I ranian Rehabilitation Journal
March 2024, Volume 22, Number 1
Review Paper
Exercise-based Rehabilitation to Improve Exercise
Tolerance of Severe COVID-19 Survivors: A Review
Paper
Arnengsih Nazir1* , Badai Bhatara Tiksnadi2 , Mochammad Farhan Fajrial Aditama Ridzki3
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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Citation Nazir A, Tiksnadi BB, MFFA Ridzki. Exercise-based Rehabilitation to Improve Exercise Tolerance of Severe COVID-19 Survivors: A Review Paper. Iranian Rehabilitation Journal. 2024; 22(1):15-24. http://dx.doi.org/10.32598/irj.22.1.1540.6
:
http://dx.doi.org/10.32598/irj.22.1.1540.6
ABSTRACT
Article info:
Received: 14 Mar 2022
Accepted: 11 Oct 2023
Available Online: 01 Mar 2024
Objectives: This review aimed to determine the form, results, and barriers to exercise-based
rehabilitation programs for severe COVID-19 survivors.
Methods: 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’]). Original articles and case
reports published in the last 2 years (July 2019-2022), written in English, available in full text,
and accessible in PDF or HTML format were included. Articles were excluded if they did not
fit the research topic after reading the full text.
Results: There were a total of 7461 articles found at the initial screening using keywords.
In the next screening using the inclusion and exclusion criteria and after reading the whole
article, we found 9 articles that matched the topic. Of these, 7 articles were original articles
and 2 case reports. All of the articles explained the forms and outcomes of exercise-based
rehabilitation in severe cases of COVID-19 survivors. However, no article explained the
barriers to rehabilitation.
Keywords:
COVID-19, Survivors,
Breathing exercises, Quality of
life, Inpatients, Outpatients
Discussion: Exercise was generally given to increase exercise tolerance in severe COVID-19
survivors in both inpatient and outpatient cardiopulmonary rehabilitation programs. The form
of exercise was aerobic, strength, or endurance training, and other forms of exercise such as
balance training as well as breathing exercises. The type and intensity of exercises given were
tailored to the patient’s needs. Research showed that exercise-based rehabilitation programs
resulted in a positive impact on increasing the survivor’s quality of life, functional capability,
and exercise tolerance. A previous study explained that barriers to rehabilitation in COVID-19
were related to the patient’s health condition, COVID-19 infectivity, and issues related to
health services.
* Corresponding Author:
Arnengsih Nazir, MD.
Address: Department of Physical Medicine and Rehabilitation, Faculty of Medicine, Dr. Hasan Sadikin General Hospital, Padjadjaran University,
Bandung, Indonesia.
Tel: +62 (81) 931222414
E-mail: arnengsih@unpad.ac.id
15
I ranian Rehabilitation Journal
March 2024, Volume 22, Number 1
Highlights
● COVID-19 survivors may experience long-term complications following the recovery of the acute phase, resulting
in a decrease in exercise tolerance.
● Exercise-based rehabilitation programs could improve the quality of life, functional capability, and exercise
tolerance of survivors.
Plain Language Summary
We reviewed the articles on forms, outcomes, and barriers of exercise-based rehabilitation programs for COVID-19
severe case survivors. The previous research found that many COVID-19 survivors experience long-term health
problems and decreased quality of life. Exercise in a rehabilitation program was given in the form of aerobics, strength,
and other exercises needed for the patients. These exercises could improve the ability of the survivors to do activities
and exercises. There was an obstacle to rehabilitation stemming from an issue related to the COVID-19 pandemic,
patient conditions, and problems related to health services.
Introduction
uscle 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].
M
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 sig-
16
nificantly 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
Nazir A, et al. Exercise-based Rehabilitation in COVID-19 Survivors. IRJ. 2024; 22(1):15-24.
I ranian Rehabilitation Journal
March 2024, Volume 22, Number 1
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
Total article search result
from PubMed
(n= 4691)
Figure 1. Article search flow
Nazir A, et al. Exercise-based Rehabilitation in COVID-19 Survivors. IRJ. 2024; 22(1):15-24.
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I ranian Rehabilitation Journal
March 2024, Volume 22, Number 1
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 train-
18
ing 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].
Nazir A, et al. Exercise-based Rehabilitation in COVID-19 Survivors. IRJ. 2024; 22(1):15-24.
I ranian Rehabilitation Journal
March 2024, Volume 22, Number 1
Table 1. Exercise-based rehabilitation for severe COVID-19 survivors
Author(s)
Title
Research
Type
Population/No. (%)/Mean±SD
COVID-19
Severity
Result of the
Form of
Rehabilitation
Rehabilitation Program
Program
Population
29
Male
20(70)
Caucasian
17(58.6)
Functional
Standard of inpatient
Median
(Range)
of
outcomes in the
60 (50.5–67.5) Severe (rerehabilitation carried Improvement of
age (y
inpatient rehaOlezene et al.
quired intuba- out by a physical thera- functional ability
bilitation setting Cohort study Most frequent
(2021) [2]
tion in an acute pist with a duration and and indepenfollowing severe
comorbidities (hy22(75.9)
phase)
frequency of at least 3
dence
COVID-19 infecpertension)
hours/day, 5x/week
tion
Obesity
18(62.1)
Dyslipidemia
16(55.2)
Mean duration of
32.2(9.3)
Population
26
Male
18(69)
The inpatient pulmoEffectiveness
Median (range) of
Severe
nary rehabilitation
Improved
66
(60–71)
of pulmonary
age (y)
(based on
program consists of
exercise perrehabilitation
Median (range) of 26.9 (24.2– WHO classifica- medical diagnostics and formance, and
Gloeckl et al. in severe and
Cohort study
tion
treatment, resistance increased lung
29.2)
BMI (kg/m2)
(2021) [15] critically ill COof COVID-19 training, strength train- capacity, muscle
VID-19 patients:
Median (range) of
severity)
ing, patient education, strength, as well
A controlled
acute care duration 37(18–60)
respiratory physiother- as quality of life
study
(d)
apy, and ADL exercises
Mean ICU care
22±85
Duration (d)
Population
28
Male
14(50)
Mean age (y)
66.04±9.3
27.6±4.9
Mean BMI (kg/m2)
Group with ventilaSignificant
12
tion
Multimodal inpatient
increase in
Group without
Feasibility and
cardiopulmonary
functional
16
ventilation
Hermann efficacy of carrehabilitation
capacity and
Severe
et al. (2020) diopulmonary Cohort study Mean duration of
of individualized
health status
19.3±10.7
[18]
rehabilitation
exercises consisting
as measured
acute care (d)
after COVID-1
of aerobic exercise by 6-MWT and
Mean duration of
and strength training
FT results
13.9±7.3
ICU care (d)
Most frequent
comorbidities
14(50)
(hypertension)
Type 2 diabetes
14(50)
Dyslipidemia
6(21.4)
Rehabilitation of
a post-intensive
Ramalingam
care unit patient
et al. (2020)
after severe
[19]
COVID-19 pneumonia
▪ Age (y)
▪ The patient
experiencing fatigue
and weakness
without symptoms
of nervous system
deficit, 2 days later
experiencing respiratory failure due to
Case report
ARDS
▪ The patient
received ICU treatment for 12 days
and then after 7
days out, he was
returned to the ICU
unit for 15 days
before undergoing
rehabilitation
64
Severe
(respiratory
failure due
to ARDS that
requires ICU
treatment)
Post-hospital discharged
rehabilitation
program independently
at home
Insignificant
which includes: 1)
increase in
Gymnastics, walking,
FIM
and climbing
Improved
stairs;
6-MWT distance
2) ROM exercises;
Improved
3) Leg strength
bilateral handtraining;
grip
4) Energy conservation;
strength
5) Diaphragmatic
breathing exercises; 6)
Walking aids;
7) Emergency
contact
Nazir A, et al. Exercise-based Rehabilitation in COVID-19 Survivors. IRJ. 2024; 22(1):15-24.
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I ranian Rehabilitation Journal
March 2024, Volume 22, Number 1
Author(s)
Title
Research
Type
Population/No. (%)/Mean±SD
Population
Effects of
comprehensive
Spielmanns pulmonary
Prospective
et al. 92021) rehabilitacohort
[20]
tion in severe
study
post-COVID-19
patients
Male
67(68)
67.72±10.23
Mean BMI (kg/m2)
28.21±6.11
Rehabilitation outcomes
Case report
for patients
Solon et al.
of 2 Caucawith severe
(2021) [22]
sian male
presentation
patients
of COVID-19: A
case series
20
54(54)
27(27)
25(25)
25(25)
Musculoskeletal
disorder
25(25)
Population
23
Male
16(70)
Mean age (y)
57±1
27±4
32±16
19±14
19(83)
11(48)
Endocrine disorder
11(48)
Type 2 diabetes
6(26)
Age
Patient 1: 82
and patient
2: 89
Patient 1: 32.7
and patient 2:
26.5
Patient 1: Hypertension,
chronic back
pain,
osteoarthritis,
history of
chronic
smoking, and
testicular
cancer
Patient 2: Hypertension,
cardiac
disorder, type
2 diabetes, hyperlipidemia,
and smoking
history
Patient 1: 18
Patient 2: 19
Comorbidities
Severe
Rehabilitation consisted
of:
Improved func1) Inpatient rehabilitational ability and
tion program; 2) Gait
ADL and aerobic
training; 3) Therapeutic
capacity based
exercises consisting of
on increased
ROM training, aero6-MWD.
bics, and endurance
exercise.
11.3±12.5
Smoker
BMI (kg/m2)
Severe
An inpatient
pulmonary
rehabilitation
An inpatient pulmonary
program with
rehabilitation program
a duration of 3
with a duration of 3
weeks consists
weeks consists of 25-30
of 25-30 sessions
sessions over 5-6 workover 5-6 working
ing days/week with
days/week with
endurance training,
endurance traingymnastics, outdoor
ing, gymnastics,
walking, strength
outdoor walking,
training, relaxation, and
strength trainrespiratory therapy
ing, relaxation,
and respiratory
therapy
25.9±8.81
Adiposities
Mean BMI (kg/m2)
Beneficial
Mean acute care
effects of multiduration (d)
disciplinary
Puchner et
rehabilitation
Mean
ICU care duraal. (2021)
Cohort study
in post-acute
tion (d)
[21]
COVID-19: An
Required mechaniobservational
cal ventilation
cohort study
Most frequent
comorbidities (cardiovascular disease)
Result of the
Form of
Rehabilitation
Rehabilitation Program
Program
99
Median age (y)
Mean duration of
acute care (d)
Mean duration of
ICU care (d)
Required oxygen
therapy
Most frequent
comorbidities (hypertension)
COVID-19
Severity
Nazir A, et al. Exercise-based Rehabilitation in COVID-19 Survivors. IRJ. 2024; 22(1):15-24.
I ranian Rehabilitation Journal
Author(s)
Title
Research
Type
March 2024, Volume 22, Number 1
Population/No. (%)/Mean±SD
Population
12 (severe and
critical cases
n=3)
Male
8(67)
Median (range) of
Feasibility of an
Betschart
acute care (d)
outpatient trainet al. (2021)
Case report
Most frequent
ing program
[23]
comorbidities (carafter COVID-19
diovascular disease)
Chronic kidney
disease
Arterial hypertonia
Cancer
Population
Male
Effectiveness
of pulmonary
Mean age (y)
rehabilitation
Büsching et
2
in severe and
al. (2021)
Cohort study Mean BMI (kg/m )
critically ill CO[24]
VID-19 patients:
Patients admitted
A controlled
to ICU
study
Patient required
intubation
Mean duration of
intubation (d)
11 (3–24)
6(50)
COVID-19
Severity
Result of the
Form of
Rehabilitation
Rehabilitation Program
Program
Mild-critical
(based on Outpatient pulmonary
Increased
WHO classifica- rehabilitation that com6-MWD result
tion
bines aerobic exercise
after rehabilitaof
(bicycle training) and
tion
COVID-19
resistance training
severity)
5(42)
3(25)
3(25)
51
38.75
65.8±11.7
27.3±4.9
30(59)
Severe and
critical
Pulmonary rehabilitation consists of cardioIncreased FIM
respiratory exercise,
and 6-MWD
strength training,
results after
relaxation techniques,
rehabilitation
and other adjunctivetherapy if needed
27(53)
13.2±7.1
Abbreviations: 6-MWD: 6-Minute walking distance; 6-MWT: 6-minute walking test; ADL: Activity of daily life; BMI: Body
mass index; WHO: World health organization; FT: Feeling thermometer; FIM: Functional independent measure; ICU: Intensive care unit; ROM: Range of motion.
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.
Nazir A, et al. Exercise-based Rehabilitation in COVID-19 Survivors. IRJ. 2024; 22(1):15-24.
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March 2024, Volume 22, Number 1
References
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
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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
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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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I ranian Rehabilitation Journal
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