Practical Recommendations Relevant to the Use of Resistance Training for COVID-19 Survivors

Abstract

The novel coronavirus disease (COVID-19) has emerged at the end of 2019 and caused a global pandemic. The disease predominantly affects the respiratory system; however, there is evidence that it is a multisystem disease that also impacts the cardiovascular system. Although the long-term consequences of COVID-19 are not well-known, evidence from similar diseases alerts for the possibility of long-term impaired physical function and reduced quality of life, especially in those requiring critical care. Therefore, rehabilitation strategies are needed to improve outcomes in COVID-19 survivors. Among the possible strategies, resistance training (RT) might be particularly interesting, since it has been shown to increase functional capacity both in acute and chronic respiratory conditions and in cardiac patients. The present article aims to propose evidence-based and practical suggestions for RT prescription for people who have been diagnosed with COVID-19 with a special focus on immune, respiratory, and cardiovascular systems. Based on the current literature, we present RT as a possible safe and feasible activity that can be time-efficient and easy to be implemented in different settings.

Full text

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HYPOTHESIS AND THEORY
published: 03 March 2021
doi: 10.3389/fphys.2021.637590
Edited by:
Robinson Ramírez-Vélez,
Public University of Navarre, Spain
Reviewed by:
Hamid Arazi,
University of Guilan, Iran
Patrik Drid,
University of Novi Sad, Serbia
José Francisco López-Gil,
University of Murcia, Spain
*Correspondence:
Paulo Gentil
paulogentil@hotmail.com
Specialty section:
This article was submitted to
Exercise Physiology,
a section of the journal
Frontiers in Physiology
Received: 03 December 2020
Accepted: 26 January 2021
Published: 03 March 2021
Citation:
Gentil P, de Lira CAB, Coswig V,
Barroso WKS, Vitorino PVdO,
Ramirez-Campillo R, Martins W and
Souza D (2021) Practical
Recommendations Relevant to the
Use of Resistance Training
for COVID-19 Survivors.
Front. Physiol. 12:637590.
doi: 10.3389/fphys.2021.637590
Practical Recommendations
Relevant to the Use of Resistance
Training for COVID-19 Survivors
Paulo Gentil1,2*, Claudio Andre Barbosa de Lira1, Victor Coswig3,
Weimar Kunz Sebba Barroso2, Priscila Valverde de Oliveira Vitorino2,4,
Rodrigo Ramirez-Campillo5,6 , Wagner Martins7and Daniel Souza1
1College of Physical Education and Dance, Federal University of Goiás, Goiânia, Brazil, 2Hypertension League, Federal
University of Goiás, Goiânia, Brazil, 3College of Physical Education, Federal University of Pará, Castanhal, Brazil, 4Social
Sciences and Health School, Pontifical Catholic University of Goiás, Goiânia, Brazil, 5Laboratory of Human Performance,
Quality of Life and Wellness Research Group, Department of Physical Activity Sciences, Universidad de Los Lagos, Osorno,
Chile, 6Centro de Investigación en Fisiología del Ejercicio, Facultad de Ciencias, Universidad Mayor, Santiago, Chile,
7Physiotherapy College, University of Brasília, Brasília, Brazil
The novel coronavirus disease (COVID-19) has emerged at the end of 2019 and caused
a global pandemic. The disease predominantly affects the respiratory system; however,
there is evidence that it is a multisystem disease that also impacts the cardiovascular
system. Although the long-term consequences of COVID-19 are not well-known,
evidence from similar diseases alerts for the possibility of long-term impaired physical
function and reduced quality of life, especially in those requiring critical care. Therefore,
rehabilitation strategies are needed to improve outcomes in COVID-19 survivors. Among
the possible strategies, resistance training (RT) might be particularly interesting, since it
has been shown to increase functional capacity both in acute and chronic respiratory
conditions and in cardiac patients. The present article aims to propose evidence-based
and practical suggestions for RT prescription for people who have been diagnosed with
COVID-19 with a special focus on immune, respiratory, and cardiovascular systems.
Based on the current literature, we present RT as a possible safe and feasible activity
that can be time-efficient and easy to be implemented in different settings.
Keywords: resistance exercise, rehabilitation, strength training, pulmonary rehabilitation, cardiac rehabilitation,
coronavirus
THE PROBLEM
The novel coronavirus disease (COVID-19) pandemic has posed a great threat to public
health concern and safety (Wu et al., 2020;Zu et al., 2020). Caused by acute respiratory
syndrome coronavirus 2 (or SARS-CoV-2), COVID-19 is characterized by respiratory distress and
multisystem disease, which is frequently severe and might result in death (Kreutz et al., 2020).
Many COVID-19 survivors who required critical care may develop psychological, physical, and
cognitive impairments (Barker-Davies et al., 2020). There is evidence that coronaviruses may
induce neurological impairments by invading the central nervous system and some patients may
have symptoms like severe muscle pain (Li Y. C. et al., 2020). COVID results in relevant morbidity
for 3–6 months (intermediate phase), and rehabilitation services and medical care might be needed
for more than 12 months (chronic phase) (Barker-Davies et al., 2020).
Previous studies showed that survivors of acute respiratory diseases might have persistent
functional disability and psychological symptoms for as much as 1 year after discharge
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(Herridge et al., 2003;Tansey et al., 2007), with most of them
showing extrapulmonary conditions, with muscle wasting and
weakness being most frequent (Herridge et al., 2003). Moreover,
many COVID-19 patients will need to be on intensive care
units, which is associated with symptoms like dyspnea, anxiety,
depression, impaired physical function, and poor quality of
life for up to 12 months after discharge (Oeyen et al., 2010;
Denehy and Elliott, 2012;Jackson et al., 2012). Among them,
physical function is one of the factors least likely to recover
to normal values as it is heavily affected by critical illness
(Gerth et al., 2019). The cardinal manifestations include limb
muscle weakness, muscle atrophy, and impairments in deep
tendon reflexes (Li Z. et al., 2020). Neuromuscular weakness
in the intensive care units can prolong the patient’s mechanical
ventilation time and hospitalization. Therefore, rehabilitation
should commence in the critical care setting, since early
exercise prevents neuromuscular complications and improves
functional status in critical illness, being considered effective,
safe, and feasible (Sosnowski et al., 2015;Barker-Davies et al.,
2020). Moreover, rehabilitation programs starting within the
post-acute phase (<30 days) seem to bring the most benefits
(Barker-Davies et al., 2020).
Besides all the knowledge about intensive care management
and recovery, there is a paucity of evidence-based
recommendations regarding rehabilitation following COVID-19.
Among the possible strategies for rehabilitating COVID-19
patients survivors, resistance training (RT) that conventionally
consists of the voluntary muscle contractions against some kind
of external resistance might be particularly interesting, since it
has been shown to be a safe and feasible strategy to increase
functional capacity in both acute and chronic respiratory
conditions (Troosters et al., 2010;Liao et al., 2015;Li et al.,
2019;Rice et al., 2020). Based on the current scientific evidence,
RT can be safe, time-efficient, and easy to be implemented in
almost anywhere and with minimal resources (Gentil et al.,
2020b;Souza et al., 2020). Therefore, the present article aims to
propose evidence-based and practical suggestions for the use of
RT for people who have been diagnosed with COVID-19 during
different phases of disease, with a special focus on immune,
respiratory, and cardiovascular systems.
IMMUNE SYSTEM
The immune system works through the coordinated functions
of many cells to protect the organism against opportunistic
infections (Pedersen and Hoffman-Goetz, 2000). Therefore,
preserving or improving its function is important for people
who were affected by COVID-19. There are evidences of either
immune surveillance or immunodepression in response to
exercise (Pedersen et al., 1998;Peake et al., 2017;Nieman and
Wentz, 2019); however, the specific effects of RT on immune
function have not being extensively studied (Freidenreich
and Volek, 2012). Interestingly, people involved in endurance
training are more commonly affected by immunodepression
and illness (Nieman, 2007) when compared to strength and
power sports (Alonso et al., 2010, 2012;Horn et al., 2010;
Timpka et al., 2017), which might be a favorable point to
RT (Natale et al., 2003;Gentil et al., 2020b). In general, the
association between exercise and body immune defenses follows
a J-shaped curve (Pedersen et al., 1998;Peake et al., 2017;
Nieman and Wentz, 2019), improving with moderate amounts of
physical exercise and decreasing with excessive or low amounts
of exercise (Pedersen et al., 1998;Peake et al., 2017;Nieman
and Wentz, 2019). This complex relation is negatively influenced
by many factors, such as higher energy expenditure (Spence
et al., 2007;Rama et al., 2013), increased exercise volume (Peters
and Bateman, 1983;Gleeson et al., 2013;Siedlik et al., 2016),
and metabolic stress (Pedersen and Hoffman-Goetz, 2000). In
this sense, an acute bout of exercise might induce a suppressive
effect on lymphocyte proliferative responses, with long-duration
(longer than 1 h) and high-intensity exercise exhibiting a
moderate suppressive effect (Siedlik et al., 2016).
A study by Davis et al. (1997) analyzed the effects of
physical exercise on susceptibility to respiratory infection by
using a murine model. The exercise design was composed
of three groups: no exercise, moderate short-term exercise
(30 min), and prolonged exercise to voluntary fatigue (2.5–
3.5 h). According to the results, exercising to fatigue resulted
in greater mortality rate (41%) than either no exercise or short-
term moderate exercise. Although mortality rate tended to be
lower after short-term moderate exercise (9%) than no exercise
(16%), there was no significant difference between conditions.
The results also showed a decrease in antiviral resistance
after strenuous exercise within the lungs, in conjunction
with increased susceptibility to respiratory infection in vivo.
Although there is paucity of data linking the transitory immune
suppression after strenuous exercise with chronic immune system
impairment and subsequently infection risk (Nieman and Wentz,
2019), it is reasonable to suggest that exercise-induced immune
suppression may impair the clearance of pathogen in acute illness
COVID-19 patients. Therefore, even after the acute phase of the
disease, physical exercise should ensure the adequate restoration
of immune defense.
For these reasons, it might be advisable to avoid strenuous
activities and adopt a reduced total training RT volume/duration
(<45 min) to preserve immune function and decrease the risk
of complications, particularly when the immune response is still
compromised (Gleeson et al., 2013;Peake et al., 2017). With that
in mind, low-volume RT should be recommended. Here, it is
important to note that training sessions lasting a few minutes
have been suggested to promote muscle strength and size gains
in different populations (Fisher J. et al., 2017;Souza et al.,
2020). From a practical standpoint, previous studies showed that
untrained young and older adults can obtain many health benefits
(e.g., increased functionality and cardiovascular improvements)
from minimal dose RT protocols involving two sets of three
to four basic exercises with a training frequency of one or two
sessions per week (Fisher et al., 2014;de Barbalho et al., 2017;
Seguro et al., 2019;Souza et al., 2019;Dias et al., 2020).
It is important to consider that rises in epinephrine,
cortisol, and sympathetic modulation seem to be related
to immunosuppression induced by exercise (Pedersen and
Hoffman-Goetz, 2000;Nieman and Wentz, 2019). In this
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regard, previous studies have shown an association between
elevated metabolic stress, cortisol levels, and immunosuppression
in response to RT (Miles et al., 2003;Ramel et al., 2003;
Krüger et al., 2011). Therefore, it might be interesting to avoid
such responses in COVID-19 survivors under rehabilitation.
According to previous studies, RT protocols with a few number of
repetitions (≤6 repetitions) and long between-sets rest intervals
(≥3 min) result in less pronounced increases in sympathetic
activity, cortisol, and lactate levels (Kraemer et al., 1990;Smilios
et al., 2003, 2007;Vale et al., 2018). Moreover, low-volume RT
with few repetitions is less glycolytic (Knuiman et al., 2015).
Therefore, it could prevent the concurrency for energy substrate
and subsequent immunosuppression, since glucose is the main
fuel of immune cells (Palmer et al., 2015).
Regarding time of the day, studies involving endurance
activities showed that the acute increases in leukocytes were
higher when exercise was performed during the night (6 PM)
when compared to morning (9 AM), and it remained high for 1 h
after exercise in a hot and humid weather (Boukelia et al., 2018).
When comparing exercise during the morning and afternoon
(9 AM vs. 4 PM) in a cold environment, Boukelia et al. (2017)
found higher immune function and less pulmonary inflammation
during afternoon exercise. We could not find specific studies with
RT; however, it has been previously shown that plasma cortisol
levels are increased during the morning (Hayes et al., 2010),
which could suggest an impaired immune function. Therefore,
the suggestion is to train in the afternoon or early night.
The basis of COVID-19 pathogenesis is associated with
a delayed antiviral response followed by an immunological
overreaction that results in an excessive proinflammatory state
(Castelli et al., 2020). The levels of systemic inflammation might
explain the severity of the disease, with the most affected patients
presenting higher serum levels of proinflammatory cytokine,
as well as reduced T lymphocytes count (Chen et al., 2020).
Regulatory T lymphocyte (Treg) is also reduced in severely ill
patients and seems to play an important role in COVID-19
pathogenesis, since it is associated with controlling autoimmune
and proinflammatory response (Gladstone et al., 2020;Stephen-
Victor et al., 2020). In this context, RT may contribute to control
proinflammatory state (Chupel et al., 2017;Santiago et al., 2018;
Lammers et al., 2020). Despite the fact that studies investigating
the effect of RT on Treg cells are scarce (Dorneles et al., 2020), a
previous study in murine model showed that RT can upregulate
this immune marker (Souza et al., 2017). Moreover, regular
practice of RT increases the levels of interleukin-10, an anti-
inflammatory cytokine that is mainly produced by Treg cells
(Chupel et al., 2017;Lammers et al., 2020).
RESPIRATORY SYSTEM
The high levels of proinflammation mediators and
histopathological changes in the lungs in response to SARS-
CoV-2 might induce apoptosis in pulmonary endothelial and
epithelial cells, leading to impaired respiratory function such
as acute respiratory distress (Castelli et al., 2020). Additionally,
persistent proinflammatory state in severe COVID-19 patients
is associated with fibroblast proliferation in the alveolar septum,
resulting in pulmonary interstitial fibrosis (Zhang et al., 2020).
Pulmonary diseases are commonly associated with loss of muscle
mass and function (Steiner, 2007;Bone et al., 2017). The analysis
of previous outbreaks of severe acute respiratory syndrome
(SARS) revealed that 6–20% of the patients showed mild or
moderate restrictive lung function consistent with muscle
weakness 6–8 weeks after hospital discharge (Chan et al., 2003).
This seems to persist for an even longer period as persistent
pulmonary function impairment was present in 37% of the
patients after recovery from SARS and their health status was
also significantly worse compared with healthy subjects (Ong
et al., 2005). Results from a cohort study showed significant
impairment in lung capacity in 23.7% of SARS survivors 1 year
after illness onset (Hui et al., 2005). Moreover, health status and
exercise capacity were remarkably lower than those found in the
normal population (Hui et al., 2005).
Previous studies showed that, in people with pulmonary
diseases, low muscle strength is associated with physical inactivity
(Osthoff et al., 2013) and is an independent predictor of
morbidity and mortality independent of the degree of respiratory
limitation (Swallow et al., 2007). Consequently, the key target
in rehabilitation for pulmonary diseases should be improving
locomotor muscle structure and function, as exercise results
in reduced benefits on exertional ventilation, operating lung
volumes, and respiratory muscle performance (Marillier et al.,
2020). Moreover, the performance of physical exercise is advised
as adjuvant non-pharmacological treatment during pulmonary
fibrosis rehabilitation (Spruit et al., 2009).
RT has been suggested as an successful strategy for pulmonary
rehabilitation, either performed alone or in conjunction with
aerobic training, since it brings important increases in functional
capacity (Liao et al., 2015;José and Dal Corso, 2016;Li et al.,
2019). It is also important to highlight that exercise training
during hospitalization due to acute respiratory conditions seems
to bring important health and functional benefits, is well
tolerated, and the adverse events are infrequent (Troosters et al.,
2010;Rice et al., 2020). RT can be successfully performed
as a stand-alone exercise strategy, without increasing adverse
events in chronic obstructive pulmonary disease patients under
pulmonary rehabilitation (Liao et al., 2015).
Considering that most people infected with SARS-CoV-2
could experience breathing difficulties, it is recommended to
control the respiratory responses to exercise. One advantage
of RT is that it might promote less cardiorespiratory stress
(i.e., oxygen consumption and pulmonary ventilation) than
aerobic exercise, even during maximal exercise testing (Houchen-
Wolloff et al., 2014;Garnacho-Castaño et al., 2015;Albesa-
Albiol et al., 2019). The manipulation of RT variables might
further reduce the respiratory stress. Pulmonary ventilation and
oxygen consumption increase with increased volume/duration
(Haddock and Wilkin, 2006;Mookerjee et al., 2016;Garnacho-
Castaño et al., 2018), lower rest intervals (Ratamess et al.,
2007;Farinatti and Castinheiras Net, 2011), higher movement
velocities (Mazzetti et al., 2011;Mukaimoto and Ohno, 2012;
Buitrago et al., 2014), and higher number of repetitions (Scott
et al., 2011;Ratamess et al., 2014). Therefore, training with
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lower number of repetitions, higher interval between sets,
and controlled movement velocity might be recommended
(Buitrago et al., 2013).
CARDIOVASCULAR SYSTEM
Similar to other coronavirus infections, COVID-19 is associated
with cardiac complications, especially arrhythmias, heart failure,
and myocardial injury (Kochi et al., 2020;Madjid et al.,
2020;Wang et al., 2020). Acute cardiac injury is higher
in those with increased mortality, with severe disease, and
requiring ventilatory support (Kochi et al., 2020;Madjid
et al., 2020). Cardiac complications have been suggested
to be multifactorial. It may be caused by hypoxia, viral
myocardial injury, hypotension, ACE2-receptor downregulation,
drug toxicity, or elevated systemic inflammation (Kochi et al.,
2020). The proinflammatory mediators associated with COVID-
19 can result in vascular inflammation, myocarditis, and
arrhythmic complications (Kochi et al., 2020;Madjid et al.,
2020). Another complication regarding cardiovascular system
is the increased risk of thromboembolism as a consequence of
coagulopathy and endothelial vascular dysfunction in critical
illness COVID-19 patients (Goshua et al., 2020).
Patients diagnosed with COVID-19 should be fully assessed
and, if necessary, additional investigations may include
resting electrocardiogram (ECG), blood exams, 24 h ECG,
cardiopulmonary, echocardiogram, cardiovascular magnetic
resonance imaging, and exercise testing with the involvement of
a cardiologist (Barker-Davies et al., 2020). In case of myocarditis,
a period of 3–6 months of complete rest from strenuous exercise
might be necessary, depending on the clinical severity illness
duration (Pelliccia et al., 2019;Schellhorn et al., 2020). After
returning, it is advisable to conduct periodic reassessment in the
first 2 years due to an increased risk of silent clinical progression
(Pelliccia et al., 2019).
RT has been shown to be safe and effective for several
cardiac patients from different cardiac diseases and has been
recommended as a core component of cardiac rehabilitation
for many decades (McKelvie and McCartney, 1990;Verrill
et al., 1992;Yamamoto et al., 2016). Some studies suggested
that RT might be even safer than aerobic exercise, since it
results in less myocardial stress and reduced hemodynamic
responses in patients with heart diseases like controlled
heart failure (Karlsdottir et al., 2002;Levinger et al., 2005),
coronary arterial disease (Karlsdottir et al., 2002), and ischemic
cardiomyopathy (McKelvie et al., 1995) and in patients in cardiac
rehabilitation after myocardial infarction and percutaneous
coronary intervention (Adams et al., 2010). Moreover, RT leads
to improvements in cardiac autonomic control of diseased
individuals (Bhati et al., 2019).
Cardiovascular stress might be more related to the duration
of the exercise than with the load used, granting the use of
higher loads and a lower number of repetitions. In this regard,
Lamotte et al. (2005) reported higher levels of blood pressure
and heart rate in response to RT using lower external loads
and higher repetitions [four sets of 17 repetitions at 40% of
the one-repetition maximum strength (1RM)] when compared
with higher external loads and lower repetitions (four sets of
10 repetitions at 70% of 1RM) in 14 patients who participated
in a rehabilitation program (e.g., bypass surgery, percutaneous
coronary angioplasty, or valvular surgery). Similarly, Gjøvaag
et al. (2016) reported higher levels of blood pressure and heart
rate in patients with coronary arterial disease after performing
15RM with lower external loads than performing 4RM with
higher external loads. Regarding autonomic modulation, Vale
et al. (2018) showed that hypertensive women training with
lower repetitions and higher external loads (6RM) showed less
sympathetic activation and higher parasympathetic activation
when compared to training with lower external loads and more
repetitions (15RM). Therefore, in order to reduce cardiovascular
stress during exercise, the recommended RT program should
involve lower number of repetitions regardless of the load used.
One important feature in previous studies is that blood
pressure and heart rate progressively increase over the sets,
especially when the rest between sets is shorter (Gotshall et al.,
1999;Lamotte et al., 2005;Gjøvaag et al., 2016). This suggests
that one should consider performing a lower number of sets
(one or two) and using higher rest between sets (≥3 min). Other
additional strategies to reduce cardiovascular stress is to give
short pauses (i.e., 5 s) in the middle of the sets (da Silva et al.,
2007;Rúa-Alonso et al., 2020), avoid performing repetitions until
muscle failure (MacDougall et al., 1992), and exercise during the
afternoon, since cardiac reactivity is lower (Jones et al., 2006;
Boukelia et al., 2018) and there is a better blood pressure control
(Jones et al., 2008) at this period of the day.
PRACTICAL RECOMMENDATIONS
RT might be performed in many settings, including acute
hospitalization and rehabilitation scenarios. Previous studies
have shown that RT performed during intensive care units
might bring important benefits either alone (Morris et al., 2016;
Barbalho et al., 2019;Veldema et al., 2019) or combined with
other activities (Eggmann et al., 2018). Interestingly, the benefits
of RT in intensive care unit patients have been reported even in
the presence of mechanical ventilation (Eggmann et al., 2018).
Another important concern with COVID-19 is the
neuropsychiatric sequalae. In addition to pandemic-associated
psychological distress, the direct and indirect effects of the
coronavirus on the human central nervous system might be
related to neuropsychiatric disorders such mood changes,
sleep disorders, depression, and anxiety (Khatoon et al., 2020;
Steardo et al., 2020;Troyer et al., 2020). Studies investigating
COVID-19 patients found a high level of post-traumatic
stress and depressive symptoms in comparison with non-
infected people (Vindegaard and Eriksen Benros, 2020). In
this regard, there are consistent evidence that RT is associated
with improvements in depression (Gordon et al., 2018), anxiety
(Gordon et al., 2017), and sleep disorders (Kovacevic et al.,
2018), including patients with chronic diseases (Ferreira et al.,
2020) and during rehabilitation (McCartney, 1998;Vincent and
Vincent, 2012;Chan and Cheema, 2016;Andrade et al., 2018;
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Seguro et al., 2019). The potential benefits of RT for COVID-19
patients are illustrated in Figure 1.
RT programs commonly involve many exercises with the
addition of isolated exercises for specific muscles, which might
be too time-consuming. However, multi-joint exercises seem to
be sufficient to improve muscle strength and hypertrophy in the
muscles involved in the exercises (Gentil et al., 2015, 2017b;Paoli
et al., 2017;Barbalho et al., 2020a,b) and there is no additional
benefits in using single-joint exercises (Gentil et al., 2013;de
França et al., 2015;Barbalho et al., 2020b). This allows the use
of multi-joint exercises combined with low-volume programs,
increasing feasibility and safety for most of the patients affected
by COVID-19, hospitalized or not, including individuals with
cardiometabolic diseases and frail elderly. Patients with COVID-
19 that present severe body aches, sore throat, shortness of breath,
chest pain, general fatigue, cough, or fever should avoid exercises
between 2 and 3 weeks after the cessation of these symptoms.
It is also recommended to avoid prolonged exhaustive or high-
intensity exercise. These current restrictions to RT practice could
be reviewed after cessation of the symptoms. COVID-19 patients
that are asymptomatic should continue to exercise, as they would
do normally. A pulmonary rehabilitation approach should be
combined in the case on return from mild/moderate COVID-19
illness (Barker-Davies et al., 2020).
RT using non-traditional equipment such as elastic devices,
which are low cost and portable, and can be performed in
almost anywhere, might contribute to increase the possibilities
for RT performance in many different settings, including
intensive care units. Previous studies reported that RT using
elastic bands or tubes resulted in similar muscle activation
and mechanical stress (Aboodarda et al., 2011, 2016), strength
gains (Martins et al., 2013), and improvements in functional
capacity (Colado et al., 2010;Souza et al., 2019) when
compared to traditional RT. Furthermore, RT might also be
performed using body weight exercises as it promotes gains in
FIGURE 1 | Multi-system benefits of resistance training.
muscle strength, hypertrophy, and body composition similar
to traditional RT for many different populations, like middle-
aged people with non-alcoholic fat liver disease (Takahashi
et al., 2015, 2017), elderly people (Tsuzuku et al., 2017),
and even young trained practitioners (Calatayud et al., 2015;
Kikuchi and Nakazato, 2017).
Another possible limitation in rehabilitation settings is the
belief that RT has to be performed with moderate to high loads
(ACSM, 2009;Kraemer et al., 2002), as it is commonly suggested
that it would be necessary to use loads ≥60% of 1RM for optimal
gains in strength and muscle mass (McDonagh and Davies, 1984;
ACSM, 2009). However, previous studies have shown that low
external load RT might bring increases in muscle fitness and
hypertrophy that are similar to conventional approaches, when
effort is high (Fisher J. P. et al., 2017;Steele et al., 2019). Previous
studies in both trained (Morton et al., 2016) and untrained people
(Mitchell et al., 2012;Assunção et al., 2016) reported that RT
with low external load resulted in similar increase in muscle
strength and hypertrophy when compared to high external load.
This is particularly evident when the strength tests not similar
to the situations trained (Fisher J. P. et al., 2017). The caveats
for using low external load are that it would require a higher
number of repetitions and longer exercise times, which can result
in more negative impact on the immune system and a higher
stress on respiratory and cardiovascular systems, as suggested
above. Therefore, the cost–benefit of such adaptations might be
analyzed individually.
Significant physiological stimulus can also be obtained
with maximal or near-maximal voluntary muscle contractions
performed without external load. In this regard, previous studies
reported high levels of muscle activation when performing
RT with the intention to maximally contract the muscles and
no external load (Gentil et al., 2017a;Alves et al., 2020).
A previous study reported equivalent gains in arm muscle
hypertrophy after traditional and no external load RT in young
men and women, using a contralateral training design (Counts
et al., 2016). Positive outcomes in terms of hypertrophy and
functionality have also been reported in intensive care units
patients (Barbalho et al., 2019).
Particularly in aging people, the performance of high-velocity
RT might be considered as an alternative strategy when the
performance of high or low external load RT with high effort
is not possible or recommended (Fragala et al., 2019). High-
velocity RT may provide superior increases on functional capacity
in comparison with conventional RT (Bottaro et al., 2007;
Nogueira et al., 2009;Ramírez-Campillo et al., 2014). A previous
study suggested that high-velocity RT might be a feasible and
safe strategy to revert or prevent functional decline during
acute hospitalization (Martínez-Velilla et al., 2019). Thus, the
performance of few repetitions using high-velocity concentric
muscle action combined with long rest intervals and/or intra-
set short pauses could provide significant gains on functionality
while preventing higher cardiovascular stress (Lamotte et al.,
2010;Dias et al., 2020). Considering that the use of light to
moderate loads (e.g., 30–60% of 1RM) are recommended to
optimize muscle power (Fragala et al., 2019), this might be
easily achieved with small implements such light dumbbells or
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FIGURE 2 | Practical recommendations for resistance training in COVID-19 survivors. ↑, higher; ↓, lower. N/A, not available.
elastic devices. Therefore, equipment and implements should
not be a barrier to implement RT programs during COVID-
19 rehabilitation.
RT progression should be based on individual analysis,
considering performance parameters and clinical symptoms.
Initially, it is recommended that progression should be
performed through increases in load, since higher number of sets
and repetitions and lower rest intervals might impose unwanted
risks. Therefore, the recommendation is to establish a repetition
margin (i.e., 4–6RM) and increase load when the participant
reaches the upper limit. When the patient reaches pre-COVID
physical capacity, it would be interesting to re-examine for the
possibility of restoring normal routine (Phelan et al., 2020).
FINAL CONSIDERATIONS
It is important to observe some general precautions for returning
to exercise post-COVID-19, like monitoring temperature before
training, starting with a muscle strengthening program prior
to cardiovascular work, keeping social distancing, observing
hygiene, adequate ventilation, and the use of masks when
necessary (So et al., 2004;Gentil et al., 2020a). Another relevant
point is the need to carefully evaluate clinical status and
supervise patients that have been diagnosed with COVID-19,
especially people with cardiac injuries (Barker-Davies et al.,
2020), highlighting the need of a multidisciplinary approach.
A subclinical myocardial injury may be present after clinical
recovery from mild infections, even without cardiac symptoms
or hospital admission. While the present article addresses RT for
rehabilitation purposes, medical clearance is required. Therefore,
a medical evaluation is recommended to exclude subclinical
diseases before resuming high-intensity training or competition,
eventually with exams such as transthoracic echocardiogram,
maximal exercise testing, and 24 h Holter monitoring (Dores and
Cardim, 2020;Wilson et al., 2020).
Considering the negligible chance of cardiac sequelae after
asymptomatic infection or local symptoms of COVID-19, it
is not necessary to perform pre-participation screening if a
critical evaluation of signs and symptoms is negative and shows
a complete recovery (Verwoert et al., 2020;Wilson et al.,
2020). However, a pre-participation screening and cardiologist
consultation may be considered for specific groups, including,
but not limited to, people with pre-existent cardiovascular
disease, elite athletes, and those with impaired recovery of
exercise capacity.
For those with regional or symptoms not requiring
hospitalization, it is strongly recommended to perform a
pre-participation screening that includes physical examination,
critical evaluation of symptoms, and a 12-lead ECG (Verwoert
et al., 2020;Wilson et al., 2020). A cardiologist experienced
in reading athletes’ ECG should be consulted to differentiate
between ECG changes due to exercise adaptation and ECG
abnormalities suggestive of cardiac disease. This is necessary
because 12-lead ECG is not the gold standard for the detection of
myocarditis. It is also recommended to use cardiac biomarkers
to detect myocarditis (Verwoert et al., 2020;Wilson et al., 2020).
However, caution should be taken when using this strategy
because most people do not have previously documented
baseline measurements to compare with, and exercise might
elevate the levels of these biomarkers, without clear-cut clinical
implications (Verwoert et al., 2020). RT may be done after
myocarditis if serum biomarkers of myocardial injury and
left ventricular systolic function are normal and if 24 h ECG
monitoring or exercise testing rules out relevant arrhythmias
(Barker-Davies et al., 2020).
It is worthy to note that most of these screening
recommendations refer to competitive athletes and high intense
activities (Dores and Cardim, 2020;Verwoert et al., 2020;Wilson
et al., 2020). Therefore, the specific limitations for performing
RT should be individually analyzed and consider the specificities
of each protocol. In this context, RT might be designed to be
especially safe for people who have been diagnosed with COVID-
19, in different stages of disease and recovery, by decreasing the
risk of immunosuppression and reducing respiratory stress and
cardiovascular risk. Interestingly, when combining the evidence
in immune, pulmonary, and cardiovascular systems, the use
of low volume/duration approaches and the manipulation of
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fphys-12-637590 February 26, 2021 Time: 14:46 # 7
Gentil et al. Resistance Training for COVID-19 Survivors
training variables (moderate to high loads, short set duration,
low number of sets, exercise choice, high rest intervals,
and/or intra-set rest) might be particularly safe (Figure 2).
RT might be also convenient as it can be performed with
different implements (traditional machines, elastic devices,
body weight exercises, or with no external load) and settings
(in-hospital, exercise facilities, or home based), increasing
its feasibility.
Finally, RT as an approach of the rehabilitation treatment
should be individualized according to the patient’s need, taking
into consideration their comorbidities, symptoms of dyspnea,
and psychological distress.
DATA AVAILABILITY STATEMENT
The raw data supporting the conclusions of this article will be
made available by the authors, without undue reservation.
AUTHOR CONTRIBUTIONS
PG and DS: conceptualization and writing the first draft. PG,
CL, VC, WB, PV, RR-C, WM, and DS: writing, review, and
editing. All authors contributed to the article and approved the
submitted version.
FUNDING
PG received a research grant from CNPq (304435/2018-0).
SUPPLEMENTARY MATERIAL
The Supplementary Material for this article can be found
online at: https://www.frontiersin.org/articles/10.3389/fphys.
2021.637590/full#supplementary-material
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Conflict of Interest: The authors declare that the research was conducted in the
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potential conflict of interest.
The handling editor declared a past co-authorship with one of the authors PG.
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