Frailty but not sarcopenia nor malnutrition increases the risk of developing COVID-19 in older community-dwelling adults
Laetitia Lengelé, Médéa Locquet, Michel Moutschen, Charlotte Beaudart, Jean-François Kaux, Sophie Gillain, Jean-Yves Reginster, Olivier Bruyère
Aging Clinical and Experimental Research, doi:10.1007/s40520-021-01991-z
Background The identification of coronavirus disease 2019 (COVID-19) risk factors is requested to implement prevention strategies. Aim To explore the associations between the COVID-19 incidence and malnutrition, sarcopenia, and frailty, identified as potential risk factors in previous cross-sectional studies. Methods Malnutrition, sarcopenia, and frailty were assessed at the last available follow-up from the Sarcopenia and Physical Impairments with Advancing Age (SarcoPhAge) cohort (i.e., the fifth year that ended in 2019) according to the Mini-Nutritional Assessment short-form, the European Working Group on Sarcopenia in Older People (EWGSOP2), and the Fried criteria, respectively. Information regarding the COVID-19 was gathered by phone calls interviews in April 2021 to measure its self-declared incidence. Adjusted Cox regressions and Kaplan-Meier curves were performed.
Results The present study included 241 participants [median age 75.6 (73.0-80.6) years, 63.1% women]. Among them, 27 participants (11.2%) developed the non-fatal Covid-19. No significant increased risks of COVID-19 were observed in patients with malnutrition [adjusted HR 1.14 (0.26-5.07)] and sarcopenia ]. Nevertheless, the incidence of COVID-19 was significantly higher in frail (44.4%) than in robust participants (8.5%) [Adjusted HR 7.01 (2.69-18.25)], which was confirmed by the Kaplan-Meier curves (p < 0.001). Among the frailty syndrome components, a low physical activity level was the only one significantly associated with an increased risk of ]. Conclusion Despite some limitations in the methodology of this study (i.e., limited sample size, COVID-19 incidence selfreported and not assessed systematically using objective measurements) requiring careful consideration, an increased risk to develop COVID-19 was observed in the presence of the frailty syndrome. Further investigations are needed to elaborate on our findings.
Supplementary Information The online version contains supplementary material available at https:// doi. org/ 10. 1007/ s40520-021-01991-z. Author contributions Conceptualization: ML, CB, J-YR, and OB; methodology: LL, ML, MM, CB, J-FK, and OB; formal analysis: LL; investigation: LL, and ML; writing-original draft preparation: LL;
Declarations
Conflict of interest The authors declare no conflict of interest.
Ethical approval The guidelines of the Declaration of Helsinki were followed, and the present study was approved by the ethics committee of the University of Liege Teaching Hospital (reference 2012/277), with two amendments in 2015 and 2018. Human and animal rights All procedures followed have been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments. Consent to participate Informed consent was obtained from all participants involved in the study. Consent for publication Informed consent was obtained from all participants involved in the study. Publisher's Note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
References
Abate, Chekole, Estifanos, Prevalence and outcomes of malnutrition among hospitalized COVID-19 patients: a systematic review and meta-analysis, Clin Nutr ESPEN,
doi:10.1016/j.clnesp.2021.03.002
Antonelli, Penfold, Merino, Risk factors and disease profile of post-vaccination SARS-CoV-2 infection in UK users of the COVID Symptom Study app: a prospective, community-based, nested, case-control study, Lancet Infect Dis,
doi:10.1016/S1473-3099(21)00460-6
Bajaj, Gadi, Spihlman, Aging, immunity, and COVID-19: how age influences the host immune response to coronavirus infections?, Front Physiol,
doi:10.3389/fphys.2020.571416
Balestroni, Bertolotti, EuroQol-5D (EQ-5D): an instrument for measuring quality of life, Monaldi Arch Chest Dis,
doi:10.4081/monaldi.2012.121
Barazzoni, Bischoff, Breda, ESPEN expert statements and practical guidance for nutritional management of individuals with SARS-CoV-2 infection, Clin Nutr,
doi:10.1016/j.clnu.2020.03.022
Beaudart, Reginster, Petermans, Quality of life and physical components linked to sarcopenia: the Sar-coPhAge study, Exp Gerontol,
doi:10.1016/j.exger.2015.05.003
Bencivenga, Rengo, Varricchi, Elderly at time of COronaVIrus disease 2019 (COVID-19): possible role of immunosenescence and malnutrition, Geroscience,
doi:10.1007/s11357-020-00218-9
Bokhorst-De, Van Der Schueren, Lonterman-Monasch, Prevalence and determinants for malnutrition in geriatric outpatients, Clin Nutr,
doi:10.1016/j.clnu.2013.05.007
Brutto, Costa, Recalde, Frailty and SARS-CoV-2 infection. A population-based study in a highly endemic village, J Neurol Sci,
doi:10.1016/j.jns.2020.117136
Cederholm, Overlaps between frailty and sarcopenia definitions, Nestle Nutr Inst Workshop Ser,
doi:10.1159/000382063
Da Silveira, Da, Fagundes, Bizuti, Physical exercise as a tool to help the immune system against COVID-19: an integrative review of the current literature, Clin Exp Med,
doi:10.1007/s10238-020-00650-3
De, Morais, Aquino, Silva-Maia, Nutritional status, diet and viral respiratory infections: perspectives for severe acute respiratory syndrome coronavirus 2, Br J Nutr,
doi:10.1017/S0007114520003311
Dumitrascu, Branje, Hladkowicz, Association of frailty with outcomes in individuals with COVID-19: a living review and meta-analysis, J Am Geriatr Soc,
doi:10.1111/jgs.17299
Folsom, Jacobs, Caspersen, Test-retest reliability of the Minnesota leisure time physical activity questionnaire, J Chronic Dis,
doi:10.1016/0021-9681(86)90195-5
Fried, Tangen, Walston, Frailty in older adults: evidence for a phenotype, J Gerontol A Biol Med Sci
Geerinck, Locquet, Bruyère, Evaluating quality of life in frailty: applicability and clinimetric properties of the SarQoL ® questionnaire, J Cachexia Sarcopenia Muscle,
doi:10.1002/jcsm.12687
Guigoz, Vellas, Nutritional assessment in older adults: MNA ® 25 years of a screening tool and a reference standard for care and research; what next ?, J Nutr Health Aging,
doi:10.1007/s12603-021-1601-y
Hanlon, Nicholl, Jani, Frailty and pre-frailty in middle-aged and older adults and its association with multimorbidity and mortality: a prospective analysis of 493 737 UK Biobank participants, Lancet Public Health,
doi:10.1016/S2468-2667(18)30091-4
Harvey, Chastin, Skelton, Prevalence of sedentary behavior in older adults: a systematic review, Int J Environ Res Public Health,
doi:10.3390/ijerph10126645
Jenkinson, The SF-36 physical and mental health summary measures: an example of how to interpret scores, J Heal Serv Res Policy,
doi:10.1177/135581969800300206
Kaiser, Bauer, Ramsch, Validation of the mini nutritional assessment short-form (MNA ® -SF): a practical tool for identification of nutritional status, J Nutr Health Aging,
doi:10.1007/s12603-009-0214-7
Kim, Yoon, Kim, Prognostic implication of baseline sarcopenia for length of hospital stay and survival in patients with coronavirus disease, J Gerontol Ser A,
doi:10.1093/gerona/glab085
Landi, Gremese, Bernabei, Post-COVID-19 global health strategies: the need for an interdisciplinary approach, Aging Clin Exp Res,
doi:10.1007/s40520-020-01616-x
Leij-Halfwerk, Verwijs, Van Houdt, Prevalence of protein-energy malnutrition risk in European older adults in community, residential and hospital settings, according to 22 malnutrition screening tools validated for use in adults ≥65 years: a systematic review and meta-analysis, Maturitas,
doi:10.1016/j.maturitas.2019.05.006
Li, Zhang, Gong, Prevalence of malnutrition and analysis of related factors in elderly patients with COVID-19 in Wuhan, China, Eur J Clin Nutr,
doi:10.1038/s41430-020-0642-3
Lidoriki, Frountzas, Schizas, Could nutritional and functional status serve as prognostic factors for COVID-19 in the elderly?, Med Hypotheses,
doi:10.1016/j.mehy.2020.109946
Lingeswaran, Goyal, Ghosh, Inflammation, immunity and immunogenetics in COVID-19: a narrative review, Indian J Clin Biochem,
doi:10.1007/s12291-020-00897-3
Ll, Ml, Mm, Cb, Ob; Resources et al., WHO Director-General's opening remarks at the media briefing on COVID-19-11
Mertens, Peñalvo, The burden of malnutrition and fatal COVID-19: a global burden of disease analysis, Front Nutr,
doi:10.3389/fnut.2020.619850
Morley, Kalantar-Zadeh, Anker, COVID-19: a major cause of cachexia and sarcopenia?, J Cachexia Sarcopenia Muscle,
doi:10.1002/jcsm.12589
Negm, Kennedy, Thabane, Management of frailty: a systematic review and network meta-analysis of randomized controlled trials, J Am Med Dir Assoc,
doi:10.1016/j.jamda.2019.08.009
Nilsson, Bergens, Kadi, Physical activity alters inflammation in older adults by different intensity levels, Med Sci Sports Exerc,
doi:10.1249/MSS.0000000000001582
O'caoimh, Sezgin, Donovan, Prevalence of frailty in 62 countries across the world: a systematic review and meta-analysis of population-level studies, Age Ageing,
doi:10.1093/ageing/afaa219
Okazaki, Ebihara, Mori, Association between sarcopenia and pneumonia in older people, Geriatr Gerontol Int,
doi:10.1111/ggi.13839
Orme, Reis, Herz, Factorial and discriminant validity of the center for epidemiological studies depression (CES-D) scale, J Clin Psychol
Richardson, Leon, Jacobs, Comprehensive evaluation of the Minnesota leisure time physical activity questionnaire, J Clin Epidemiol,
doi:10.1016/0895-4356(94)90008-6
Roberts, Denison, Martin, A review of the measurement of grip strength in clinical and epidemiological studies: towards a standardised approach, Age Ageing,
doi:10.1093/ageing/afr051
Rubenstein, Harker, Salvà, Screening for undernutrition in geriatric practice: developing the short-form mini-nutritional assessment (MNA-SF), J Gerontol,
doi:10.1093/gerona/56.6.M366
Shafiee, Keshtkar, Soltani, Prevalence of sarcopenia in the world: a systematic review and meta-analysis of general population studies, J Diabetes Metab Disord,
doi:10.1186/s40200-017-0302-x
Sierra, Bossuyt, Braeye, All-cause mortality supports the COVID-19 mortality in Belgium and comparison with major fatal events of the last century, Arch Public Heal,
doi:10.1186/s13690-020-00496-x
Sofra, Badami, Adverse effects of sedentary lifestyles: inflammation, and high-glucose induced oxidative stress-a double blind randomized clinical trial on diabetic and prediabetic patients, Health,
doi:10.4236/health.2020.128076
Streicher, Van Zwienen-Pot, Bardon, Determinants of incident malnutrition in community-dwelling older adults: a Manuel multicohort meta-analysis, J Am Geriatr Soc,
doi:10.1111/jgs.15553
Suardi, Cazzaniga, Graci, Link between viral infections, immune system, inflammation and diet, Int J Environ Res Public Health,
doi:10.3390/ijerph18052455
Vellas, Villars, Abellan, Overview of the MNA ® -its history and challenges, J Nutr Heal Aging
Wierdsma, Kruizenga, Konings, Poor nutritional status, risk of sarcopenia and nutrition related complaints are prevalent in COVID-19 patients during and after hospital admission, Clin Nutr ESPEN,
doi:10.1016/j.clnesp.2021.03.021
Willows, Alam, Sandhu, A Canadian perspective on severe acute respiratory syndrome coronavirus 2 infection and treatment: how prevalent underlying inflammatory disease contributes to pathogenesis, Biochem Cell Biol,
doi:10.1139/bcb-2020-0341
Woolford, Angelo, Curtis, COVID-19 and associations with frailty and multimorbidity: a prospective analysis of UK Biobank participants, Aging Clin Exp Res,
doi:10.1007/s40520-020-01653-6
Wu, Chen, Cai, Risk factors associated with acute respiratory distress syndrome and death in patients with coronavirus disease 2019 pneumonia in Wuhan, China, JAMA Intern Med,
doi:10.1001/jamainternmed.2020.0994
Wu, Lewis, Pae, Nutritional modulation of immune function: analysis of evidence, mechanisms, and clinical relevance, Front Immunol,
doi:10.3389/fimmu.2018.03160
Wyper, Assunção, Cuschieri, Population vulnerability to COVID-19 in Europe: a burden of disease analysis, Arch Public Heal,
doi:10.1186/s13690-020-00433-y
Yu, Ye, Chen, Erratum to: malnutrition prolongs the hospitalization of patients with COVID-19 infection: a clinical epidemiological analysis (The journal of nutrition, health and aging, J Nutr Heal Aging