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Covid-19 and the impact on the physical activity level of elderly people: A systematic review

Introduction Social isolation and lifestyle changes provoked by the COVID-19 pandemic have negatively affected the level of physical activity of the elderly people. Objective To evaluate the available evidence related to the level of physical activity (PA) of elderly people during the COVID-19 pandemic. Methods This is a systematic review, registered on PROSPERO (CRD42021241116), which included cross-sectional and cohort studies. Embase, Pubmed, Cochrane, Web of Science and Scopus databases were used to search for the studies. Finally, the New Castle-Ottawa Quality Assessment scale was used to measure the quality of the studies. Results 25 studies were found, being 14 cross-sectional and 11 cohort studies. The studies showed that the elderly population was highly affected in relation to the level of physical activity and lifestyle during restrictions, quarantine and lockdowns caused by the COVID-19. There was a significant reduction in physical activity levels, leading to declines in physical fitness and increased sedentary lifestyle, factors directly related to the increase in frailty in this population. Conclusion The level of physical activity in the elderly population decreased during the quarantine period of COVID-19 worldwide. Strategies to maintain physical condition must be encouraged with physical exercises that meets the needs of the elderly in the current pandemic scenario, in order to maintain and improve the health of this population.


Introduction
The SARS-CoV-2 virus, originated in China in December 2019, spread around the world causing a catastrophic pandemic, which led to the collapse of the healthcare systems in several countries and caused millions of deaths (Johns Hopkins University, 2021;World Health Organization Report, 2020). Because it has a high potential for transmission between humans, mainly by aerosols (WHO, 2020a), several government restrictions involving social distancing were created around the world, as a strategy to contain the COVID-19 outbreak (Centers for Disease Control and Prevention (CDC), 2020).
The positive results of these measures leave no doubt that social distancing reduces the transmission of the virus (Matrajt and Leung, 2020;Wang et al., 2020a). However, it is equally undeniable that such restrictions have harmed the quality of life and reduced the levels of physical activity (PA) of the global population (Martinez et al., 2020;Stockwell et al., 2021), leading to concerns secondary to the pandemic (Hall et al., 2021). The World Health Organization defines PA as "any bodily movement produced by skeletal muscles that required energy expenditure", and determines the quantity of PA that must be performed by age groups (WHO, 2020b). For elderly people, it is recommended to do at least 150-300 min of moderate-intensity aerobic PA or at least 75-150 min or vigorous-intensity aerobic PA throughout the week (WHO, 2020b).
The need for social distancing during the COVID-19 pandemic has resulted in drastic changes in lifestyle and social behavior (Hall et al., 2021). This leads to abrupt physical inactivity, which is associated not only with a reduction in skeletal muscle mass, but also with a loss of strength, which is an independent risk factor for mortality (Newman et al., 2006).
In an observational study including a total of 117 elderly people, conducted to investigate the influence of six weeks of lockdown on PA levels, perceived physical function, and mood of people aged ≥70 years, Richardson et al. (2021) found a significant increase in the time of sedentary behavior during the period of restrictions, which is related to negative impacts on health.
In addition to that, the increase in sedentary behavior during the pandemic is expected to lead to significant reductions in musculoskeletal strength and endurance and in cardiorespiratory capacity. Also concerning is the loss of lean mass, muscle function and motor control, that can lead to sarcopenia, cardiometabolic disorders and the emergence and/or worsening of other comorbidities, with more significant impacts on the elderly (Pelicioni and Lord, 2020;Rodrigues et al., 2020;Roschel et al., 2020). All of these factors lead to functional decline, which culminates in limitations in daily life and increased risk of falls, which can lead to serious trauma (Pérez-Ros et al., 2019), increasing morbidity and mortality rates (Rodrigues et al., 2020), especially in the elderly population (19 e 22).
Given the above, it is undeniable that social distance policies and changes in lifestyle during the COVID-19 pandemic have negatively affected the physical health of the elderly. Such losses bring concerns to the post-pandemic period, as the current scenario shows an increase in sedentary behavior and in the body mass index (Ekelund et al., 2019), which is associated with several diseases such as high blood pressure, diabetes, cardiovascular and respiratory diseases, among others (Lin et al., 2019;Powell-Wiley et al., 2021;Ten Hacken, 2009;Ahima, 2009).
In this sense, with a focus on elucidating the current evidence on this topic, the aim of this systematic review was to assess the available evidence related to the level of PA of the elderly people during the COVID-19 pandemic. We hypothesized that the elderly population was severely affected in relation to the level of PA during restrictions, quarantines and lockdowns caused by the COVID-19 pandemic.

Study design and ethical approval
This systematic review was performed based on Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) (Page et al., 2020;Page et al., 2021) guidelines, specific for observational studies. The review was prospectively registered on PROSPERO (registration number: CRD42021241116).

Inclusion and exclusion criteria
The following inclusion criteria were considered in this review:

Search strategy
The search for studies was systematically performed in October 2021, at the following databases, via Capes Periodicals (https://www.pe riodicos.capes.gov.br/): 1) Embase; 2) PubMed; 3) Cochrane; 4) Web of Science; and 5) Scopus. The English terms used in the search were based on the literature corresponding to the purpose of the systematic review and on the encyclopedia of Medical Subject Headings (MeSH) terms. The primary descriptor "physical exercise" and its similar descriptors (e.g., "physical activity"; "sedentary behavior") was crossed with the secondary descriptors "elderly" and its similar ones (e.g. "older adults"; "aged") and "COVID-19".
The search only restricted the following factors: "publication period", defined from December 2019, when the first cases of COVID-19 appeared in China, until the day the search was carried out (October 2021); and "study type", including only complete observational studies. Other factors such as language and type of access (free or paid) were not restricted.
The manual search was performed based on the reference lists of the selected articles and on the simple search on the databases mentioned above.

Study selection
Two reviewers (IPS and VMK) independently performed the selection of the studies based on titles, abstracts and descriptors/keywords of all studies identified by the search strategy, according to the PRISMA guidelines (Page et al., 2020;Page et al., 2021). In case of disagreement, a third reviewer (e.g., MRO) was included as a tiebreaker (screening phase).
Subsequently, two reviewers (IPS and VMK) fully read all the preselected studies according to the eligibility criteria, where the same tiebreaker strategy was adopted as described in the previous phase (eligibility phase). The software State of the Art Through Systematic Reviews (StArt) (Luís et al., 2016) was used to conduct the study selection process.

Extract data and bias assessment
Finally, the data extraction was performed by two reviewers (IPS and VMK) independently regarding the characteristics of the studies and participants, assessment method of PA levels and main outcomes (inclusion phase).
The assessment of methodological quality was performed by two reviewers (IPS and VMK), following the New Castle -Ottawa Quality Assessment Scale for Cohort Studies and adapted for Cross-Sectional Studies, that contemplates three categories (Selection, Comparability and Outcomes) (Wells et al., n.d.). Studies with Newcastle-Ottawa form scores (Stang, 2010) of ≥7 were considered as high-quality, 5-6 as moderate quality and 0-4 as low-quality studies.

Selection of the studies
A total of 1328 studies were found by searching the following databases: PubMed (165), Scopus (199), Web of Science (349), Cochrane library (47) and Embase (568). After excluding duplicate articles (442) and studies not meeting the inclusion criteria based on titles and abstracts (794), 92 studies showed potential relevance for full analysis. However, only 25 studies met the predefined eligibility criteria (14 cross-sectional and 11 cohort studies) ( Figure 1).

Study characteristics
The characteristics of the studies included in this systematic review are described in Table 1. Regarding the nationality of the studies found, a prevalence of Japan, Spain and Italy was observed. Because the studies evaluated PA levels during the COVID-19 pandemic, all articles are recently published (from 2020 to 2021). The total number of individuals evaluated, including samples of all studies, was 15,964 elderly subjects. In most studies, the female gender was predominant. Few studies addressed comorbidities, with arterial hypertension, Parkinson's disease and diabetes mellitus being the most prevalent.

Main results of the studies
The methods for assessing the PA level and the main results of the studies are described in Table 2. The studies found aimed to evaluate and compare the levels of PA during the COVID-19 pandemic and lockdowns and to demonstrate the clinical impact of this period on the health of the elderly population.
Regarding the instruments used in the studies to assess the PA level, the International Physical Activity Questionnaire (IPAQ) predominated, either in its full, short (IPAQ-SF), or Environment Module (IPAQ-E) form. In addition, studies also used the Physical Activity Scale for the Elderly (PASE) questionnaire and the accelerometer.
From the application of such instruments, the authors found that quarantine and restrictions to prevent the spread of COVID-19 induced a significant reduction in PA levels in both sexes and changes in lifestyle. The main causes of the reduction in the level of PA, mentioned by the studies, in this period were the increase in sitting time, reduction in equivalent metabolic tasks (METs) and decrease in the number of steps. In addition, there was a reduction in exercise frequency and duration. Tables 3 and 4 show the quality of the 25 studies included, classified based on the Newcastle-Ottawa Quality Assessment Scale for cohort studies and the adapted scale for cross sectional studies (Wells et al., n. d.).

Discussion
The studies included in this systematic review confirmed the hypothesis that the elderly population had the PA levels affected during restrictions, quarantines and lockdowns due to the COVID-19 pandemic, regardless of the country of origin of the study, given that each country followed its sanitary rules. The studies showed that there was a reduction in PA levels in the elderly due to the increase in sitting time, reduction in METs and decrease of the number of steps, which can lead to a decline in physical fitness and an increase in sedentary lifestyle. Maugeri et al. (2020) showed a significant reduction in the total energy for weekly PA of the elderly in Italy. Pérez et al. (2021) in Spain, Meyer et al. (2020) in USA, Qin et al. (2020) in China and Yamada et al. (2020Yamada et al. ( , 2021 in Japan found similar data, each one in their countries. Such data point to a PA reduction at a global level, reinforcing the need to develop strategies to change this condition, regardless of the country of origin. However, although the studies in this systematic review showed that the elderly people had PA levels affected by the pandemic independently in the country of origin of the study, it is important to emphasize that majority of the studies included in this systematic review were conducted in Europe and Asia (21 of 25 studies).
Both continents (Europe and Asia) suffered drastically with the COVID-19 pandemic and had high infection rates in 2020. Not coincidentally, countries in these continents had more severe social distancing and quarantine policies (China's aggressive measures have slowed the coronavirus, 2020; Woskie et al., 2021), which surely affected the lifestyle of these populations. This can be observed by the infection and mortality rates worldwide. Currently, the American continent leads the ranking of infections and mortality by COVID-19 (COVID-19 ranking, n. d.), which reflects the most flexible social distancing policies in these countries, especially in the United States and Brazil. Asia and Europe adopted early and aggressive social distancing policies to contain the outbreak (China's aggressive measures have slowed the coronavirus, 2020; Woskie et al., 2021), and despite there is no clear evidence comparing the impact of these policies between countries worldwide on PA levels, this leads us to the understanding that these measures had a greater impact on mobility and lifestyle of the European and Asian population when comparing to other continents.
It is noteworthy that during the period when the study of Browne et al. (2020) was carried out, Brazil was experiencing a partial blockage of outdoor activities in many regions of the country, and the fact that this study assessed elderly people, allows us to clarify the results found. As the mortality rate was high in elderly and considering the daily disclosure by the media in relation to the number of deaths as well as the "stay at home" recommendations, this population may have had an even more severe impact on the reduction of the level of physical activity in relation to other age groups, favoring an increase in sedentary behavior, corroborating the findings of the Browne et al. (2020) study. In addition, in the study by Miyahara et al. (2021), carried out in Japan, in which they used accelerometers to objectively measure physical activity, the government officials imposed strict rules for the lockdown, affecting the level of physical activity, as shown by the results. On the other hand, in Sweden study, it is known that the impact of lockdowns and government-imposed blocks was smaller, with no impact on the level of M.R. Oliveira et al. Experimental Gerontology 159 (2022) 111675 physical activity of the elderly, as shown in the study by Leavy et al. (2021).
In addition to the reduction in PA level, studies also associated this with other factors, such as frailty, pointed out by Shinohara et al. (2021). The worse self-perception of health reported by the elderly indicated a greater frailty, and those who were aware of a decrease in their lower limb muscle strength were significantly more fragile (Shinohara et al., 2021). Makizako et al. (2021) also underscore this decline in health perception and associate lower rates of exercise with a decline in cognitive function during a state of emergency.
Therefore, the pandemic not only caused a reduction in the level of PA in this population, but also the self-perception of health, muscle strength and cognitive function, which may result in irreversible consequences in this critical period. It is still not possible to state the reasons why this level of PA has decreased, requiring studies with better methodological quality and validated assessments. These studies should consider personal, environmental and other factors that may influence the level of PA and should be better studied as potential preventive aspects and intervention targets.
It is known the importance of physical exercise in the elderly. Cunningham et al. (2020) and McPhee et al. (2016) identified that physically active elderly people have a reduced risk of cardiovascular mortality, breast and prostate cancer, fractures, limitations in activities of daily living (ADLs), functional limitations, risk of falls, cognitive declines and depression. In addition, the active elderly also experiences healthier aging trajectories and better quality of life. The authors also emphasize that starting with small increases in PA can encourage this population to progressively incorporate more activities into their daily routine (Cunningham et al., 2020;McPhee et al., 2016). Oliveira et al. (2020) corroborate that there is an association between PA and prevention of frailty and sarcopenia. Thus, encouraging physical exercise and PA in the elderly in this pandemic period becomes essential. Hammami et al. (2020) complemented that for optimal health, dietary guidelines must be combined with a physically active lifestyle and that during the prolonged "stay at home" policies, regular activity hours were changed, leading to an increase in sedentary behavior. The study also suggests that, currently, exercise is crucial, as PA is capable of improving sleep quality, mood and attenuating the manifestations of stress and anxiety, increased by social isolation. In addition, exercising at an appropriate intensity is associated with better immune system responses against viral respiratory infections (Hammami et al., 2020). Chen et al. (2021) propose that the immunological hypothesis for the vulnerability of COVID-19 in the elderly involves an age-related impairment of the immune defense (immunosenescence) and consequently an increased risk of immunopathology.
Curiously, despite the fact that the elderly population is more susceptible to suffer from COVID-19, being a high-risk population for the disease, there is evidence that higher ages may not turn the elderly more likely to isolate, when compared to people with 50 to 60 years old (Daoust, 2020). However, it is important to mention that the minimum social isolation may have greater impact in elderly people, especially when it comes to decreases in PA and functional capacity, since it is already known that muscle mass decreases 3 to 8% per decade after the age of 30 and it comes even worse after de age of 60 (Volpi et al., 2004).
Regarding the methodological quality of the studies, most of the cross-sectional studies were classified as "moderate quality", whereas for the cohort studies, "low quality" methodologies were prevalent, mainly because the studies did not perform the selection and comparability recommendations as suggested by the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) (Von Elm       , 2007). However, since COVID-19 is a new disease, which still needs further studies for its better understanding, this preliminary evidence was able to provide important information to direct strategies for the development of exercise protocols focused on the elderly population, which lack scientific support at the current time.
There are limitations in our systematic review that must be considered. Among them, there is a bias in the subjectivity of the responses to the questionnaires in relation to the level of PA and referred symptoms applied in the included studies, as these are often self-reported. In addition, the heterogeneity of the measures of the studies found can be mentioned, which limits the use of more robust methods for the synthesis of results. Also, due to the fact that this review includes observational studies (cross-sectional and cohort), we cannot confirm these data, as they do not prove cause and effect. However, it is important to highlight that we seek the best evidence, with validated assessments and that COVID-19 is a new disease and we still have many gaps that only time will allow scientists and researchers to answer. As it is a recent and relevant topic at the moment, the results of the present study may provide important contribution to clinical practice, given the scarcity of data to guide health professionals.
Furthermore, we must consider that the included studies did not classify individuals according to their PA level before and after the pandemic, however, few studies used gold standard measures to objectively measure physical activity (i.e. accelerometers). Finally, the most of studies did not report the severity of the lockdown imposed in each region in which the study was developed in order to consider the impact of lockdown in the active behavior and if some physical approaches were made to attenuate these changes. Therefore, we recommend that future studies consider the points above mentioned so that more consistent analyzes can confirm the findings of active behavior impairment caused by the COVID-19 pandemic.

Clinical implications
Since the end of 2019 the general population and mainly the elderly have been suffering from the loss of public spaces, such as gyms, physiotherapy clinics, outdoor leisure areas and social exercise groups. As a consequence, the present systematic review showed the reduction in the PA levels, with studies consistently showing this reduction mainly from the IPAQ (increase in sitting time and reduction in the amount of METs)  and accelerometry (reduction in the number of steps). This is an important factor for the loss of muscle strength, mobility, balance, cardiorespiratory endurance, functional independence, increased depression index and, consequently, increased frailty syndrome in the elderly (Battaglia et al., 2014;Bellafiore et al., 2011;Cesari et al., 2015;O'Connor et al., 1993). All these consequences are related to an increased risk of mortality.
As an alternative, in times of PA restriction due to the pandemic, home and outdoor exercises can maintain and improve the health and fitness of the elderly, given the decrease in PA levels observed in this population, as seen in this systematic review. Finally, Chen et al. (2021) suggest that exercise supervision, whether through weekly visits or telephone calls, is recommended to improve the effects of exercise at home and reduce the risk of falls.
Thus, this review provides data to guide health professionals, such as geriatricians, physiotherapists, physical educators, nutritionists and health assistants, to focus on the need to implement/maintain exercise promotion, reducing functional losses during the pandemic of COVID-19 and to encourage the continuity of activities and physical exercise safely, in order to maintain their healthy lifestyle and, consequently, improve their autonomy and quality of life.

Conclusion
The level of PA in the elderly population decreased during the quarantine period of COVID-19 worldwide. The increase in sitting time, reduction in the amount of METs and the decrease in the number of steps were important factors for the reduction of PA levels. However, most studies presented a low to moderate methodological quality and assessed the level of PA through questionnaires, which may underestimate the findings. Therefore, more accurate methods to assess PA levels in the elderly and clinical studies to find the cause and effect of symptoms are needed in future studies.
In addition, strategies to maintain physical condition must be developed with exercise protocols and interventions that match the needs of the elderly in the current pandemic scenario, in order to maintain/improve the health, muscle strength, cognitive function and, consequently, quality of life of the elderly population.

Funding acknowledgement
This study is supported by a research grant by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-Brasil (CAPES -001) and by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq). Audrey Borghi-Silva is an established Investigator (level IB) of the CNPq, Brazil.

Declaration of competing interest
No potential conflict of interest was reported by the authors.

Table 4
Quality assessments for cohort studies included (NEWCASTLE-OTTAWA QUALITY ASSESSMENT SCALE).

Selection
Comparability Outcome Total Score Representativeness of the exposed cohort Selection of the nonexposed cohort