Physical Activity Modifies the Severity of COVID-19 in Hospitalized Patients—Observational Study
Edyta Sutkowska, Agata Stanek, Katarzyna Madziarska, Grzegorz K Jakubiak, Janusz Sokołowski, Marcin Madziarski, Karolina Sutkowska-Stępień, Karolina Biernat, Justyna Mazurek, Adrianna Borowkow-Bulek, Jakub Czyżewski, Gabriela Wilk, Arkadiusz Jagasyk, Dominik Marciniak
Journal of Clinical Medicine, doi:10.3390/jcm12124046
Background and aim: Physical activity (PA) can modulate the immune response, but its impact on infectious disease severity is unknown. We assess if the PA level impacts the severity of COVID-19. Methods: Prospective, cohort study for adults hospitalized due to COVID-19, who filled out the International Physical Activity Questionnaire (IPAQ). Disease severity was expressed as death, transfer to intensive care unit (ICU), oxygen therapy (OxTh), hospitalization length, complications, C-reactive protein, and procalcitonin level. Results: Out of 326 individuals, 131 (57; 43.51% women) were analyzed: age: median-70; range: 20-95; BMI: mean-27.18 kg/m 2 ; and SD: ±4.77. During hospitalization: 117 (83.31%) individuals recovered, nine (6.87%) were transferred to ICU, five (3.82%) died, and 83 (63.36%) needed OxTh. The median for the hospital stay was 11 (range: 3-49) for discharged patients, and mean hospitalization length was 14 (SD: ±5.8312) for deaths and 14.22 days (SD: ±6.92) for ICU-transferred patients. The median for MET-min/week was 660 (range: 0-19,200). Sufficient or high PA was found in recovered patients but insufficient PA was observed in dead or ICU-transferred patients (p = 0.03). The individuals with poor PA had a higher risk of death (HR = 2.63; ±95%CI 0.58-11.93; p = 0.037). OxTh was used more often in the less active individuals (p = 0.03). The principal component analysis confirmed a relationship between insufficient PA and an unfavorable course of the disease. Conclusion: A higher level of PA is associated with a milder course of COVID-19.
Informed Consent Statement: Informed consent was obtained from all subjects involved in the study. 
 Conflicts of Interest: The authors declare no conflict of interest.
References
Biernat, Stupnicki, Gajewski, International Physical Activity Questionnaire (IPAQ)-Polish version, Wych Fiz. Spor
Biscarini, Colaneri, Ludovisi, Seminari, Pieri et al., The obesity paradox: Analysis from the SMAtteo COvid-19 REgistry (SMACORE) cohort, Nutr. Metab. Cardiovasc. Dis, 
doi:10.1016/j.numecd.2020.07.047 
Chandarana, Pisuchpen, Krieger, Dane, Mikheev et al., Association of body composition parameters measured on CT with risk of hospitalization in patients with Covid-19, Eur. J. Radiol
Chen, Stevinson, Ku, Chang, Chu, Relationships of leisure-time and non-leisure-time physical activity with depressive symptoms: A population-based study of Taiwanese older adults, Int. J. Behav. Nutr. Phys. Act
Craig, Marshall, Sjöström, Bauman, Booth et al., International physical activity questionnaire: 12-country reliability and validity, Med. Sci. Sports Exerc, 
doi:10.1249/01.MSS.0000078924.61453.FB 
De Sanctis, Ruggiero, Soliman, Daar, Di Maio et al., Coronavirus Disease 2019 (COVID-19) in adolescents: An update on current clinical and diagnostic characteristics, Acta Biomed, 
doi:10.23750/abm.v91i2.9543 
Denay, Breslow, Turner, Nieman, Roberts et al., ACSM call to action statement: COVID-19 considerations for sports and physical activity, Curr. Sports Med. Rep, 
doi:10.1249/JSR.0000000000000739 
Dutra, Da-Silva, Mineo, Turner, Editorial: The effects of physical activity and exercise on immune responses to infection, Front. Immunol, 
doi:10.3389/fimmu.2022.842568 
Fezeu, Julia, Henegar, Bitu, Hu et al., Obesity is associated with higher risk of intensive care unit admission and death in influenza A (H1N1) patients: A systematic review and meta-analysis, Obes. Rev, 
doi:10.1111/j.1467-789X.2011.00864.x 
Jakobsson, Cotgreave, Furberg, Arnberg, Svensson, Potential physiological and cellular mechanisms of exercise that decrease the risk of severe complications and mortality following SARS-CoV-2 infection. Sports 2021, 
doi:10.3390/sports9090121 
Lan, Chang, Tai, Relationship between components of leisure physical activity and mortality in Taiwanese older adults, Prev. Med, 
doi:10.1016/j.ypmed.2006.03.016 
Lim, Lee, Jeong, Han, Association of Physical Activity with SARS-CoV-2 Infection and Severe Clinical Outcomes Among Patients in South Korea, JAMA Netw. Open, 
doi:10.1001/jamanetworkopen.2023.9840 
Martinez-Gomez, Guallar-Castillon, Garcia-Esquinas, Bandinelli, Rodríguez-Artalejo, Physical activity and the effect of multimorbidity on all-cause mortality in older adults, Mayo Clin. Proc, 
doi:10.1016/j.mayocp.2016.12.004 
Molanorouzi, Khoo, Morris, Motives for adult participation in physical activity: Type of activity, age, and gender, 
doi:10.1186/s12889-015-1429-7 
Myers, Kokkinos, Nyelin, Physical activity, cardiorespiratory fitness, and the metabolic syndrome, Nutrients, 
doi:10.3390/nu11071652 
Nieman, Coronavirus disease-2019: A tocsin to our aging, unfit, corpulent, and immunodeficient society, J. Sport Health Sci, 
doi:10.1016/j.jshs.2020.05.001 
Nieman, Exercise Is Medicine for Immune Function: Implication for COVID-19, Curr. Sports Med. Rep
Novotová, Pavl Ů, Dvořáčková, Arnal-Gómez, Espí-López, Influence of walking as physiological training to improve respiratory parameters in the elderly population, Int. J. Environ. Res. Public Health, 
doi:10.3390/ijerph19137995 
Posadzki, Pieper, Bajpai, Makaruk, Könsgen et al., Exercise/physical activity and health outcomes: An overview of Cochrane systematic reviews, BMC Public Health, 
doi:10.1186/s12889-020-09855-3 
Puciato, Sociodemographic associations of physical activity in people of working age, Int. J. Environ. Res. Public Health, 
doi:10.3390/ijerph16122134 
Romero Starke, Reissig, Petereit-Haack, Schmauder, Nienhaus et al., The isolated effect of age on the risk of COVID-19 severe outcomes: A systematic review with meta-analysis, BMJ Glob, 
doi:10.1136/bmjgh-2021-006434 
Rothschild, Islam, Bishop, Kilding, Stewart et al., Factors influencing AMPK activation during cycling exercise: A pooled analysis and meta-regression, Sports Med, 
doi:10.1007/s40279-021-01610-x 
Rottoli, Bernante, Belvedere, Balsamo, Garelli et al., How important is obesity as a risk factor for respiratory failure, intensive care admission and death in hospitalised COVID-19 patients? Results from a single Italian centre, Eur. J. Endocrinol, 
doi:10.1530/EJE-20-0541 
Rütten, Vuillemin, Ooijendijk, Schena, Sjöströmet et al., Physical activity monitoring in Europe. The European Physical Activity Surveillance System (EUPASS) approach and indicator testing, Public Health Nutr, 
doi:10.1079/PHN2002449 
Schnohr, O'keefe, Marott, Lange, Jensen, Dose of jogging and long-term mortality: The Copenhagen City Heart Study, J. Am. Coll. Cardiol, 
doi:10.1016/j.jacc.2014.11.023 
Simonnet, Chetboun, Poissy, Raverdy, Noulette et al., High prevalence of obesity in severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2) requiring invasive mechanical ventilation, Obesity, 
doi:10.1002/oby.22831 
Vancampfort, Koyanagi, Ward, Rosenbaum, Schuch et al., Chronic physical conditions, multimorbidity and physical activity across 46 low-and middle-income countries, Int. J. Behav. Nutr. Phys. Act, 
doi:10.1186/s12966-017-0463-5 
Wu, Chen, Cai, Xia, Zhou et al., Risk factors associated with acute respiratory distress syndrome and death in patients with coronavirus disease, JAMA Intern. Med, 
doi:10.1001/jamainternmed.2020.0994 
Yang, Ding, Zou, Shen, Hu et al., Visceral adiposity and high intramuscular fat deposition independently predict critical illness in patients with SARS-CoV-2, Obesity, 
doi:10.1002/oby.22971 
DOI record:
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  "abstract": "<jats:p>Background and aim: Physical activity (PA) can modulate the immune response, but its impact on infectious disease severity is unknown. We assess if the PA level impacts the severity of COVID-19. Methods: Prospective, cohort study for adults hospitalized due to COVID-19, who filled out the International Physical Activity Questionnaire (IPAQ). Disease severity was expressed as death, transfer to intensive care unit (ICU), oxygen therapy (OxTh), hospitalization length, complications, C-reactive protein, and procalcitonin level. Results: Out of 326 individuals, 131 (57; 43.51% women) were analyzed: age: median—70; range: 20–95; BMI: mean—27.18 kg/m²; and SD: ±4.77. During hospitalization: 117 (83.31%) individuals recovered, nine (6.87%) were transferred to ICU, five (3.82%) died, and 83 (63.36%) needed OxTh. The median for the hospital stay was 11 (range: 3–49) for discharged patients, and mean hospitalization length was 14 (SD: ±5.8312) for deaths and 14.22 days (SD: ±6.92) for ICU-transferred patients. The median for MET-min/week was 660 (range: 0–19,200). Sufficient or high PA was found in recovered patients but insufficient PA was observed in dead or ICU-transferred patients (p = 0.03). The individuals with poor PA had a higher risk of death (HR = 2.63; ±95%CI 0.58–11.93; p = 0.037). OxTh was used more often in the less active individuals (p = 0.03). The principal component analysis confirmed a relationship between insufficient PA and an unfavorable course of the disease. Conclusion: A higher level of PA is associated with a milder course of COVID-19.</jats:p>",
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    {
      "DOI": "10.1016/S0140-6736(20)30183-5",
      "article-title": "Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China",
      "author": "Huang",
      "doi-asserted-by": "crossref",
      "first-page": "497",
      "journal-title": "Lancet",
      "key": "ref_1",
      "volume": "395",
      "year": "2020"
    },
    {
      "DOI": "10.1530/EJE-20-0541",
      "article-title": "How important is obesity as a risk factor for respiratory failure, intensive care admission and death in hospitalised COVID-19 patients? Results from a single Italian centre",
      "author": "Rottoli",
      "doi-asserted-by": "crossref",
      "first-page": "389",
      "journal-title": "Eur. J. Endocrinol.",
      "key": "ref_2",
      "volume": "183",
      "year": "2020"
    },
    {
      "DOI": "10.1001/jamainternmed.2020.0994",
      "article-title": "Risk factors associated with acute respiratory distress syndrome and death in patients with coronavirus disease 2019 pneumonia in Wuhan, China",
      "author": "Wu",
      "doi-asserted-by": "crossref",
      "first-page": "1031",
      "journal-title": "JAMA Intern. Med.",
      "key": "ref_3",
      "volume": "180",
      "year": "2020"
    },
    {
      "DOI": "10.1136/bmjgh-2021-006434",
      "article-title": "The isolated effect of age on the risk of COVID-19 severe outcomes: A systematic review with meta-analysis",
      "author": "Reissig",
      "doi-asserted-by": "crossref",
      "first-page": "e006434",
      "journal-title": "BMJ Glob. Health",
      "key": "ref_4",
      "volume": "6",
      "year": "2021"
    },
    {
      "DOI": "10.1186/s12889-015-1429-7",
      "doi-asserted-by": "crossref",
      "key": "ref_5",
      "unstructured": "Molanorouzi, K., Khoo, S., and Morris, T. (2015). Motives for adult participation in physical activity: Type of activity, age, and gender. BMC Public Health, 15."
    },
    {
      "DOI": "10.3390/ijerph16122134",
      "doi-asserted-by": "crossref",
      "key": "ref_6",
      "unstructured": "Puciato, D. (2019). Sociodemographic associations of physical activity in people of working age. Int. J. Environ. Res. Public Health, 16."
    },
    {
      "article-title": "Coronavirus Disease 2019 (COVID-19) in adolescents: An update on current clinical and diagnostic characteristics",
      "author": "Ruggiero",
      "first-page": "184",
      "journal-title": "Acta Biomed.",
      "key": "ref_7",
      "volume": "91",
      "year": "2020"
    },
    {
      "DOI": "10.1186/s12889-020-09855-3",
      "doi-asserted-by": "crossref",
      "key": "ref_8",
      "unstructured": "Posadzki, P., Pieper, D., Bajpai, R., Makaruk, H., Könsgen, N., Neuhaus, A.L., and Semwal, M. (2020). Exercise/physical activity and health outcomes: An overview of Cochrane systematic reviews. BMC Public Health, 20."
    },
    {
      "DOI": "10.1016/j.ypmed.2006.03.016",
      "article-title": "Relationship between components of leisure physical activity and mortality in Taiwanese older adults",
      "author": "Lan",
      "doi-asserted-by": "crossref",
      "first-page": "36",
      "journal-title": "Prev. Med.",
      "key": "ref_9",
      "volume": "43",
      "year": "2006"
    },
    {
      "DOI": "10.1017/S1368980099000567",
      "article-title": "The influence of physical activity on mental well-being",
      "author": "Fox",
      "doi-asserted-by": "crossref",
      "first-page": "411",
      "journal-title": "Public Health Nutr.",
      "key": "ref_10",
      "volume": "2",
      "year": "1999"
    },
    {
      "DOI": "10.1186/1479-5868-9-28",
      "article-title": "Relationships of leisure-time and non-leisure-time physical activity with depressive symptoms: A population-based study of Taiwanese older adults",
      "author": "Chen",
      "doi-asserted-by": "crossref",
      "first-page": "28",
      "journal-title": "Int. J. Behav. Nutr. Phys. Act.",
      "key": "ref_11",
      "volume": "14",
      "year": "2012"
    },
    {
      "DOI": "10.1016/j.it.2020.11.002",
      "article-title": "T cells: Warriors of SARS-CoV-2 infection",
      "author": "Prattichizzo",
      "doi-asserted-by": "crossref",
      "first-page": "18",
      "journal-title": "Trends Immunol.",
      "key": "ref_12",
      "volume": "42",
      "year": "2021"
    },
    {
      "DOI": "10.1038/s41591-020-01202-8",
      "article-title": "Immune determinants of COVID-19 disease presentation and severity",
      "author": "Brodin",
      "doi-asserted-by": "crossref",
      "first-page": "28",
      "journal-title": "Nat. Med.",
      "key": "ref_13",
      "volume": "27",
      "year": "2021"
    },
    {
      "DOI": "10.1016/j.cell.2021.01.007",
      "article-title": "Adaptive immunity to SARS-CoV-2 and COVID-19",
      "author": "Sette",
      "doi-asserted-by": "crossref",
      "first-page": "861",
      "journal-title": "Cell",
      "key": "ref_14",
      "volume": "184",
      "year": "2021"
    },
    {
      "DOI": "10.3389/fimmu.2022.842568",
      "article-title": "Editorial: The effects of physical activity and exercise on immune responses to infection",
      "author": "Dutra",
      "doi-asserted-by": "crossref",
      "first-page": "842568",
      "journal-title": "Front. Immunol.",
      "key": "ref_15",
      "volume": "13",
      "year": "2022"
    },
    {
      "DOI": "10.1016/j.jshs.2018.09.009",
      "article-title": "The compelling link between physical activity and the body’s defense system",
      "author": "Nieman",
      "doi-asserted-by": "crossref",
      "first-page": "201",
      "journal-title": "J. Sport Health Sci.",
      "key": "ref_16",
      "volume": "8",
      "year": "2019"
    },
    {
      "DOI": "10.1249/JSR.0000000000000739",
      "article-title": "ACSM call to action statement: COVID-19 considerations for sports and physical activity",
      "author": "Denay",
      "doi-asserted-by": "crossref",
      "first-page": "326",
      "journal-title": "Curr. Sports Med. Rep.",
      "key": "ref_17",
      "volume": "19",
      "year": "2020"
    },
    {
      "DOI": "10.1016/j.jshs.2020.05.001",
      "article-title": "Coronavirus disease-2019: A tocsin to our aging, unfit, corpulent, and immunodeficient society",
      "author": "Nieman",
      "doi-asserted-by": "crossref",
      "first-page": "293",
      "journal-title": "J. Sport Health Sci.",
      "key": "ref_18",
      "volume": "9",
      "year": "2020"
    },
    {
      "DOI": "10.1002/jmv.26232",
      "article-title": "The cytokine storm and COVID-19",
      "author": "Hu",
      "doi-asserted-by": "crossref",
      "first-page": "250",
      "journal-title": "J. Med. Virol.",
      "key": "ref_19",
      "volume": "93",
      "year": "2021"
    },
    {
      "DOI": "10.1249/JSR.0000000000000867",
      "article-title": "Exercise Is Medicine for Immune Function: Implication for COVID-19",
      "author": "Nieman",
      "doi-asserted-by": "crossref",
      "first-page": "395",
      "journal-title": "Curr. Sports Med. Rep.",
      "key": "ref_20",
      "volume": "20",
      "year": "2021"
    },
    {
      "DOI": "10.1007/s40279-021-01610-x",
      "article-title": "Factors influencing AMPK activation during cycling exercise: A pooled analysis and meta-regression",
      "author": "Rothschild",
      "doi-asserted-by": "crossref",
      "first-page": "1273",
      "journal-title": "Sports Med.",
      "key": "ref_21",
      "volume": "52",
      "year": "2022"
    },
    {
      "DOI": "10.3389/fendo.2022.879066",
      "article-title": "Irisin, exercise, and COVID-19",
      "author": "Alves",
      "doi-asserted-by": "crossref",
      "first-page": "879066",
      "journal-title": "Front. Endocrinol.",
      "key": "ref_22",
      "volume": "13",
      "year": "2022"
    },
    {
      "DOI": "10.1016/j.jshs.2019.12.003",
      "article-title": "Exercise immunology: Future directions",
      "author": "Nieman",
      "doi-asserted-by": "crossref",
      "first-page": "432",
      "journal-title": "J. Sport Health Sci.",
      "key": "ref_23",
      "volume": "9",
      "year": "2020"
    },
    {
      "DOI": "10.1016/j.jacc.2014.11.023",
      "article-title": "Dose of jogging and long-term mortality: The Copenhagen City Heart Study",
      "author": "Schnohr",
      "doi-asserted-by": "crossref",
      "first-page": "411",
      "journal-title": "J. Am. Coll. Cardiol.",
      "key": "ref_24",
      "volume": "65",
      "year": "2015"
    },
    {
      "DOI": "10.3390/nu11071652",
      "doi-asserted-by": "crossref",
      "key": "ref_25",
      "unstructured": "Myers, J., Kokkinos, P., and Nyelin, E. (2019). Physical activity, cardiorespiratory fitness, and the metabolic syndrome. Nutrients, 11."
    },
    {
      "DOI": "10.1249/01.MSS.0000078924.61453.FB",
      "article-title": "International physical activity questionnaire: 12-country reliability and validity",
      "author": "Craig",
      "doi-asserted-by": "crossref",
      "first-page": "1381",
      "journal-title": "Med. Sci. Sports Exerc.",
      "key": "ref_26",
      "volume": "35",
      "year": "2003"
    },
    {
      "article-title": "International Physical Activity Questionnaire (IPAQ)-Polish version",
      "author": "Biernat",
      "first-page": "47",
      "journal-title": "Wych Fiz. Spor.",
      "key": "ref_27",
      "volume": "51",
      "year": "2007"
    },
    {
      "DOI": "10.1079/PHN2002449",
      "article-title": "Physical activity monitoring in Europe. The European Physical Activity Surveillance System (EUPASS) approach and indicator testing",
      "author": "Vuillemin",
      "doi-asserted-by": "crossref",
      "first-page": "377",
      "journal-title": "Public Health Nutr.",
      "key": "ref_28",
      "volume": "6",
      "year": "2003"
    },
    {
      "DOI": "10.1055/s-2000-8847",
      "article-title": "Exercise and insulin sensitivity: A review",
      "author": "Borghouts",
      "doi-asserted-by": "crossref",
      "first-page": "302",
      "journal-title": "Int. J. Sports Med.",
      "key": "ref_29",
      "volume": "21",
      "year": "2000"
    },
    {
      "DOI": "10.1152/physrev.90100.2007",
      "article-title": "Muscle as an endocrine organ: Focus on muscle-derived interleukin-6",
      "author": "Pedersen",
      "doi-asserted-by": "crossref",
      "first-page": "1379",
      "journal-title": "Physiol. Rev.",
      "key": "ref_30",
      "volume": "88",
      "year": "2008"
    },
    {
      "key": "ref_31",
      "unstructured": "(2022, June 12). IPAQ International Physical Activity Questionaire. Available online: https://www.physio-pedia.com/images/c/c7/Quidelines_for_interpreting_the_IPAQ.pdf."
    },
    {
      "DOI": "10.3390/ijerph19137995",
      "doi-asserted-by": "crossref",
      "key": "ref_32",
      "unstructured": "Novotová, K., Pavlů, D., Dvořáčková, D., Arnal-Gómez, A., and Espí-López, G.V. (2022). Influence of walking as physiological training to improve respiratory parameters in the elderly population. Int. J. Environ. Res. Public Health, 19."
    },
    {
      "key": "ref_33",
      "unstructured": "(2022, November 10). Available online: https://virtual.cvot.org/wp-content/uploads/2022/11/CVOT_Summit_2022_Programme_Booklet.pdf."
    },
    {
      "DOI": "10.1016/j.mayocp.2016.12.004",
      "article-title": "Physical activity and the effect of multimorbidity on all-cause mortality in older adults",
      "author": "Bandinelli",
      "doi-asserted-by": "crossref",
      "first-page": "376",
      "journal-title": "Mayo Clin. Proc.",
      "key": "ref_34",
      "volume": "92",
      "year": "2017"
    },
    {
      "DOI": "10.1186/s12966-017-0463-5",
      "article-title": "Chronic physical conditions, multimorbidity and physical activity across 46 low-and middle-income countries",
      "author": "Vancampfort",
      "doi-asserted-by": "crossref",
      "first-page": "6",
      "journal-title": "Int. J. Behav. Nutr. Phys. Act.",
      "key": "ref_35",
      "volume": "14",
      "year": "2017"
    },
    {
      "DOI": "10.1016/bs.pmbts.2015.08.001",
      "article-title": "Exercise and the regulation of immune functions",
      "author": "Simpson",
      "doi-asserted-by": "crossref",
      "first-page": "355",
      "journal-title": "Prog. Mol. Biol. Transl. Sci.",
      "key": "ref_36",
      "volume": "135",
      "year": "2015"
    },
    {
      "DOI": "10.1111/j.1467-789X.2011.00864.x",
      "article-title": "Obesity is associated with higher risk of intensive care unit admission and death in influenza A (H1N1) patients: A systematic review and meta-analysis",
      "author": "Fezeu",
      "doi-asserted-by": "crossref",
      "first-page": "653",
      "journal-title": "Obes. Rev.",
      "key": "ref_37",
      "volume": "12",
      "year": "2011"
    },
    {
      "DOI": "10.1016/j.numecd.2020.07.047",
      "article-title": "The obesity paradox: Analysis from the SMAtteo COvid-19 REgistry (SMACORE) cohort",
      "author": "Biscarini",
      "doi-asserted-by": "crossref",
      "first-page": "1920",
      "journal-title": "Nutr. Metab. Cardiovasc. Dis.",
      "key": "ref_38",
      "volume": "30",
      "year": "2020"
    },
    {
      "DOI": "10.1002/oby.22831",
      "article-title": "High prevalence of obesity in severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2) requiring invasive mechanical ventilation",
      "author": "Simonnet",
      "doi-asserted-by": "crossref",
      "first-page": "1195",
      "journal-title": "Obesity",
      "key": "ref_39",
      "volume": "28",
      "year": "2020"
    },
    {
      "DOI": "10.1002/oby.22971",
      "article-title": "Visceral adiposity and high intramuscular fat deposition independently predict critical illness in patients with SARS-CoV-2",
      "author": "Yang",
      "doi-asserted-by": "crossref",
      "first-page": "2040",
      "journal-title": "Obesity",
      "key": "ref_40",
      "volume": "28",
      "year": "2020"
    },
    {
      "DOI": "10.1016/j.ejrad.2021.110031",
      "article-title": "Association of body composition parameters measured on CT with risk of hospitalization in patients with Covid-19",
      "author": "Chandarana",
      "doi-asserted-by": "crossref",
      "first-page": "110031",
      "journal-title": "Eur. J. Radiol.",
      "key": "ref_41",
      "volume": "145",
      "year": "2021"
    },
    {
      "DOI": "10.3390/sports9090121",
      "doi-asserted-by": "crossref",
      "key": "ref_42",
      "unstructured": "Jakobsson, J., Cotgreave, I., Furberg, M., Arnberg, N., and Svensson, M. (2021). Potential physiological and cellular mechanisms of exercise that decrease the risk of severe complications and mortality following SARS-CoV-2 infection. Sports, 9."
    },
    {
      "DOI": "10.1001/jamanetworkopen.2023.9840",
      "article-title": "Association of Physical Activity with SARS-CoV-2 Infection and Severe Clinical Outcomes Among Patients in South Korea",
      "author": "Lim",
      "doi-asserted-by": "crossref",
      "first-page": "e239840",
      "journal-title": "JAMA Netw. Open",
      "key": "ref_43",
      "volume": "6",
      "year": "2023"
    }
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