[en] Muscle weakness and physical performance impairment are common geriatric conditions that raise morbidity and mortality. They are known to be affected by nutrition, but only a few longitudinal studies exist. This study aims to fill this gap by exploring the association, over 3 years, between variations of nutrient intakes, as well as, on one side, the variations of handgrip strength, as a surrogate of muscle strength, and on the other side, the physical performance, assessed by gait speed. Participants from the SarcoPhAge study, a Belgian cohort of people aged 65 years and older, were asked to complete a self-administered food frequency questionnaire (FFQ) at the second (T2) and the fifth (T5) year of follow-up. Daily macro- and micronutrient intakes were measured and their changes in consumption over the three years of follow-up were then calculated. The association between changes in nutrients consumption and the variations in muscle parameters were investigated through multiple linear regressions. Out of the 534 participants included in the cohort, 238 had complete data at T2 and T5 (median age of 72.0 years (70.0-78.0 years), 60.9% women). In the cross-sectional analysis, calories, omega-3 fatty acids, potassium, and vitamins D, A, and K intakes were positively correlated with muscle strength. In the longitudinal analysis, neither the gait speed nor the muscle strength changes were significantly impacted by the variations. Other longitudinal investigations with longer follow-up are required to improve knowledge about these interrelations.
Disciplines :
Public health, health care sciences & services Endocrinology, metabolism & nutrition
Author, co-author :
Lengele, Laetitia ; Université de Liège - ULiège > Département des sciences de la santé publique > Santé publique, Epidémiologie et Economie de la santé
Moehlinger, Pauline
Bruyère, Olivier ; Université de Liège - ULiège > Département des sciences de la santé publique > Santé publique, Epidémiologie et Economie de la santé
Locquet, Médéa ; Université de Liège - ULiège > Département des sciences de la santé publique > Epidémiologie clinique
Reginster, Jean-Yves ; Université de Liège - ULiège > Département des sciences de la santé publique > Santé publique, Epidémiologie et Economie de la santé
Beaudart, Charlotte ; Université de Liège - ULiège > Département des sciences de la santé publique > Santé publique, Epidémiologie et Economie de la santé
Language :
English
Title :
Association between Changes in Nutrient Intake and Changes in Muscle Strength and Physical Performance in the SarcoPhAge Cohort.
Publication date :
2020
Journal title :
Nutrients
ISSN :
2072-6643
Publisher :
Multidisciplinary Digital Publishing Institute (MDPI), Switzerland
Ponti, F.; Santoro, A.; Mercatelli, D.; Gasperini, C.; Conte, M.; Martucci, M.; Sangiorgi, L.; Franceschi, C.; Bazzocchi, A. Aging and Imaging Assessment of Body Composition: From Fat to Facts. Front. Endocrinol. 2020, 10. [CrossRef] [PubMed]
Tangen, G.G.; Robinson, H.S. Measuring physical performance in highly active older adults: Associations with age and gender? Aging Clin. Exp. Res. 2020, 32, 229–237. [CrossRef] [PubMed]
Cruz-Jentoft, A.J.; Bahat, G.; Bauer, J.; Boirie, Y.; Bruyère, O.; Cederholm, T.; Cooper, C.; Landi, F.; Rolland, Y.; Sayer, A.A.; et al. Sarcopenia: Revised European consensus on definition and diagnosis. Age Ageing 2019, 48, 16–31. [CrossRef] [PubMed]
Auyeung, T.W.; Lee, S.W.J.; Leung, J.; Kwok, T.; Woo, J. Age-associated decline of muscle mass, grip strength and gait speed: A 4-year longitudinal study of 3018 community-dwelling older Chinese. Geriatr. Gerontol. Int. 2014, 14, 76–84. [CrossRef]
Goodpaster, B.H.; Park, S.W.; Harris, T.B.; Kritchevsky, S.B.; Nevitt, M.; Schwartz, A.V.; Simonsick, E.M.; Tylavsky, F.A.; Visser, M.; Newman, A.B. The Loss of Skeletal Muscle Strength, Mass, and Quality in Older Adults: The Health, Aging and Body Composition Study. J. Gerontol. 2006, 61, 1059–1064. [CrossRef]
Kuo, H.-K.; Leveille, S.G.; Yen, C.-J.; Chai, H.-M.; Chang, C.-H.; Yeh, Y.-C.; Yu, Y.-H.; Bean, J.F. Exploring How Peak Leg Power and Usual Gait Speed Are Linkedto Late-Life Disability: Data from the National Health and Nutrition Examination Survey (NHANES), 1999-2002. Am. J. Phys. Med. Rehabil. 2006, 85, 650–658. [CrossRef]
Hardy, S.E.; Perera, S.; Roumani, Y.F.; Chandler, J.M.; Studenski, S.A. Improvement in usual gait speed predicts better survival in older adults. J. Am. Geriatr. Soc. 2007, 55, 1727–1734. [CrossRef]
Roberts, H.C.; Syddall, H.E.; Cooper, C.; Aihie sayer, A. Is grip strength associated with length of stay in hospitalised older patients admitted for rehabilitation? Findings from the Southampton grip strength study. Age Ageing 2012, 41, 641–646. [CrossRef]
Leong, D.P.; Teo, K.K.; Rangarajan, S.; Lopez-Jaramillo, P.; Avezum, A.; Orlandini, A.; Seron, P.; Ahmed, S.H.; Rosengren, A.; Kelishadi, R.; et al. Prognostic value of grip strength: Findings from the Prospective Urban Rural Epidemiology (PURE) study. Lancet 2015, 386, 266–273. [CrossRef]
De Rekeneire, N.; Visser, M.; Peila, R.; Nevitt, M.C.; Cauley, J.A.; Tylavsky, F.A.; Simonsick, E.M.; Harris, T.B. Is a Fall Just a Fall: Correlates of Falling in Healthy Older Persons. The Health, Aging and Body Composition Study. J. Am. Geriatr. Soc. 2003, 51, 841–846. [CrossRef] [PubMed]
Studenski, S.; Perera, S.; Wallace, D.; Chandler, J.M.; Duncan, P.W.; Rooney, E.; Fox, M.; Guralnik, J.M. Physical Performance Measures in the Clinical Setting. J. Am. Geriatr. Soc. 2003, 51, 314–322. [CrossRef] [PubMed]
Penninx, B.W.J.H.; Ferrucci, L.; Leveille, S.G.; Rantanen, T.; Pahor, M.; Guralnik, J.M. Lower Extremity Performance in Nondisabled Older Persons as a Predictor of Subsequent Hospitalization. J. Gerontol. 2000, 55, 691–697. [CrossRef]
Hajek, A.; Brettschneider, C.; Eisele, M.; Kaduszkiewicz, H.; Mamone, S.; Wiese, B.; Weyerer, S.; Werle, J.; Fuchs, A.; Pentzek, M.; et al. Correlates of hospitalization among the oldest old: Results of the AgeCoDe–AgeQualiDe prospective cohort study. Aging Clin. Exp. Res. 2020, 32, 1295–1301. [CrossRef]
Mijnarends, D.M.; Luiking, Y.C.; Halfens, R.J.G.; Evers, S.M.A.A.; Lenaerts, E.L.A.; Verlaan, S.; Wallace, M.; Schols, J.M.G.A.; Meijers, J.M.M. Muscle, Health and Costs: A Glance at their Relationship. J. Nutr. Health Aging 2018, 22, 766–773. [CrossRef] [PubMed]
Guerra, R.S.; Amaral, T.F.; Sousa, A.S.; Pichel, F.; Restivo, M.T.; Ferreira, S.; Fonseca, I. Handgrip strength measurement as a predictor of hospitalization costs. Eur. J. Clin. Nutr. 2015, 69, 187–192. [CrossRef]
Tieland, M.; Trouwborst, I.; Clark, B.C. Skeletal muscle performance and ageing. J. Cachexia Sarcopenia Muscle 2018, 9, 3–19. [CrossRef]
Landi, F.; Camprubi-Robles, M.; Bear, D.E.; Cederholm, T.; Malafarina, V.; Welch, A.A.; Cruz-Jentoft, A.J. Muscle loss: The new malnutrition challenge in clinical practice. Clin. Nutr. 2019, 38, 2113–2120. [CrossRef]
Corcoran, C.; Murphy, C.; Culligan, E.P.; Walton, J.; Sleator, R.D. Malnutrition in the elderly. Sci. Prog. 2019, 102, 171–180. [CrossRef]
Volkert, D.; Beck, A.M.; Cederholm, T.; Cereda, E.; Cruz-Jentoft, A.; Goisser, S.; de Groot, L.; Großhauser, F.; Kiesswetter, E.; Norman, K.; et al. Management of Malnutrition in Older Patients—Current Approaches, Evidence and Open Questions. J. Clin. Med. 2019, 8, 974. [CrossRef] [PubMed]
Adly, N.N.; Abd-El-Gawad, W.M.; Abou-Hashem, R.M. Relationship between malnutrition and different fall risk assessment tools in a geriatric in-patient unit. Aging Clin. Exp. Res. 2020, 32, 1279–1287. [CrossRef] [PubMed]
Roy, M.; Gaudreau, P.; Payette, H. A scoping review of anorexia of aging correlates and their relevance to population health interventions. Appetite 2016, 105, 688–699. [CrossRef] [PubMed]
Landi, F.; Lattanzio, F.; Dell’Aquila, G.; Eusebi, P.; Gasperini, B.; Liperoti, R.; Belluigi, A.; Bernabei, R.; Cherubini, A. Prevalence and potentially reversible factors associated with anorexia among older nursing home residents: Results from the ulisse project. J. Am. Med. Dir. Assoc. 2013, 14, 119–124. [CrossRef]
Jadczak, A.D.; Visvanathan, R. Anorexia of Aging—An Updated Short Review. J. Nutr. Health Aging 2019, 23, 306–309. [CrossRef]
Landi, F.; Calvani, R.; Tosato, M.; Martone, A.M.; Ortolani, E.; Savera, G.; Sisto, A.; Marzetti, E. Anorexia of aging: Risk factors, consequences, and potential treatments. Nutrients 2016, 8, 69. [CrossRef] [PubMed]
Volkert, D.; Kiesswetter, E.; Cederholm, T.; Donini, L.M.; Eglseer, D.; Norman, K.; Schneider, S.M.; Ströbele-Benschop, N.; Torbahn, G.; Wirth, R.; et al. Development of a Model on Determinants of Malnutrition in Aged Persons: A MaNuEL Project. Gerontol. Geriatr. Med. 2019, 5, 233372141985843. [CrossRef]
Ter Borg, S.; Verlaan, S.; Hemsworth, J.; Mijnarends, D.M.; Schols, J.M.G.A.; Luiking, Y.C.; De Groot, L.C.P.G.M. Micronutrient intakes and potential inadequacies of community-dwelling older adults: A systematic review. Br. J. Nutr. 2015, 113, 1195–1206. [CrossRef]
Jensen, G.L.; Cederholm, T. The malnutrition overlap syndromes of cachexia and sarcopenia: A malnutrition conundrum. Am. J. Clin. Nutr. 2018, 108, 1157–1158. [CrossRef]
Beaudart, C.; Sanchez-Rodriguez, D.; Locquet, M.; Reginster, J.Y.; Lengelé, L.; Bruyère, O. Malnutrition as a strong predictor of the onset of sarcopenia. Nutrients 2019, 11, 2883. [CrossRef]
Amarya, S.; Singh, K.; Sabharwal, M. Changes during aging and their association with malnutrition. J. Clin. Gerontol. Geriatr. 2015, 6, 78–84. [CrossRef]
Deutz, N.E.P.; Ashurst, I.; Ballesteros, M.D.; Bear, D.E.; Cruz-Jentoft, A.J.; Genton, L.; Landi, F.; Laviano, A.; Norman, K.; Prado, C.M. The Underappreciated Role of Low Muscle Mass in the Management of Malnutrition. J. Am. Med. Dir. Assoc. 2019, 20, 22–27. [CrossRef] [PubMed]
Beaudart, C.; Locquet, M.; Touvier, M.; Reginster, J.Y.; Bruyère, O. Association between dietary nutrient intake and sarcopenia in the SarcoPhAge study. Aging Clin. Exp. Res. 2019, 31, 815–824. [CrossRef] [PubMed]
McLean, R.R.; Mangano, K.M.; Hannan, M.T.; Kiel, D.P.; Sahni, S. Dietary Protein Intake Is Protective Against Loss of Grip Strength Among Older Adults in the Framingham Offspring Cohort. J. Gerontol. Ser. A Biol. Sci. Med. Sci. 2016, 71, 356–361. [CrossRef]
Granic, A.; Mendonça, N.; Sayer, A.A.; Hill, T.R.; Davies, K.; Adamson, A.; Siervo, M.; Mathers, J.C.; Jagger, C. Low protein intake, muscle strength and physical performance in the very old: The Newcastle 85+ Study. Clin. Nutr. 2018, 37, 2260–2270. [CrossRef]
Visser, M.; Deeg, D.J.H.; Lips, P. Low Vitamin D and High Parathyroid Hormone Levels as Determinants of Loss of Muscle Strength and Muscle Mass (Sarcopenia): The Longitudinal Aging Study Amsterdam. J. Clin. Endocrinol. Metab. 2003, 88, 5766–5772. [CrossRef]
Houston, D.K.; Tooze, J.A.; Neiberg, R.H.; Hausman, D.B.; Johnson, M.A.; Cauley, J.A.; Bauer, D.C.; Cawthon, P.M.; Shea, M.K.; Schwartz, G.G.; et al. 25-hydroxyvitamin D status and change in physical performance and strength in older adults. Am. J. Epidemiol. 2012, 176, 1025–1034. [CrossRef]
Fingeret, M.; Vollenweider, P.; Marques-Vidal, P. No association between vitamin C and E supplementation and grip strength over 5 years: The Colaus study. Eur. J. Nutr. 2019, 58, 609–617. [CrossRef]
Granic, A.; Mendonça, N.; Hill, T.R.; Jagger, C.; Stevenson, E.J.; Mathers, J.C.; Sayer, A.A. Nutrition in the very old. Nutrients 2018, 10, 269. [CrossRef]
Giezenaar, C.; Chapman, I.; Luscombe-Marsh, N.; Feinle-Bisset, C.; Horowitz, M.; Soenen, S. Ageing is associated with decreases in appetite and energy intake—A meta-analysis in healthy adults. Nutrients 2016, 8, 28. [CrossRef]
JafariNasabian, P.; Inglis, J.E.; Reilly, W.; Kelly, O.J.; Ilich, J.Z. Aging human body: Changes in bone, muscle and body fat with consequent changes in nutrient intake. J. Endocrinol. 2017, 234, R37–R51. [CrossRef] [PubMed]
Peters, D.M.; Fritz, S.L.; Krotish, D.E. Assessing the reliability and validity of a shorter walk test compared with the 10-Meter Walk Test for measurements of gait speed in healthy, older adults. J. Geriatr. Phys. Ther. 2013, 36, 24–30. [CrossRef] [PubMed]
Schaap, L.A.; Fox, B.; Henwood, T.; Bruyère, O.; Reginster, J.Y.; Beaudart, C.; Buckinx, F.; Roberts, H.; Cooper, C.; Cherubini, A.; et al. Grip strength measurement: Towards a standardized approach in sarcopenia research and practice. Eur. Geriatr. Med. 2016, 7, 247–255. [CrossRef]
Arnault, N. Table de Composition des Aliments, étude NutriNet-Santé. [Food Composition Table, NutriNet-Santé Study]; Les éditions INSERM: Paris, France, 2013.
Taylor, H.L.; Jacobs, D.R.; Schucker, B.; Knudsen, J.; Leon, A.S.; Debacker, G. A questionnaire for the assessment of leisure time physical activities. J. Chronic Dis. 1978, 31, 741–755. [CrossRef]
Vetrano, D.L.; Landi, F.; Volpato, S.; Corsonello, A.; Meloni, E.; Bernabei, R.; Onder, G. Association of sarcopenia with short-and long-term mortality in older adults admitted to acute care wards: Results from the CRIME study. J. Gerontol. Ser. A Biol. Sci. Med. Sci. 2014, 69, 1154–1161. [CrossRef]
Steffl, M.; Bohannon, R.W.; Petr, M.; Kohlikova, E.; Holmerova, I. Relation between cigarette smoking and sarcopenia: Meta-analysis. Physiol. Res. 2015, 64, 419–426. [CrossRef]
Dallongeville, J.; Maré, N.; Fruchart, J.-C.; Amouyel, P. Community and International Nutrition Cigarette Smoking Is Associated with Unhealthy Patterns of Nutrient Intake: A Meta-analysis. J. Nutr. 1998, 128, 1450–1457. [CrossRef]
Zadak, Z.; Hyspler, R.; Ticha, A.; Vlcek, J. Polypharmacy and malnutrition. Curr. Opin. Clin. Nutr. Metab. Care 2013, 16, 50–55. [CrossRef]
Streicher, M.; van Zwienen-Pot, J.; Bardon, L.; Nagel, G.; Teh, R.; Meisinger, C.; Colombo, M.; Torbahn, G.; Kiesswetter, E.; Flechtner-Mors, M.; et al. Determinants of Incident Malnutrition in Community-Dwelling Older Adults: A MaNuEL Multicohort Meta-Analysis. J. Am. Geriatr. Soc. 2018, 66, 2335–2343. [CrossRef]
Beaudart, C.; Reginster, J.Y.; Petermans, J.; Gillain, S.; Quabron, A.; Locquet, M.; Slomian, J.; Buckinx, F.; Bruyère, O. Quality of life and physical components linked to sarcopenia: The SarcoPhAge study. Exp. Gerontol. 2015, 69, 103–110. [CrossRef]
Thiébaut, A.; Kesse, E.; Com-Nougué, C.; Clavel-Chapelon, F.; Bénichou, J. Ajustement sur l’apport énergétique dans l’évaluation des facteurs de risque alimentaires Adjustment for energy intake in the assessment of dietary risk factors. Rev. Epidemiol. Sante Publique 2004, 52, 539–557.
Conseil Supérieur de la Santé (CSS). Recommandations Nutritionnelles Pour la Belgique 2016; CSSAvis n◦9285: Bruxelles, Belgium, 2016.
Wysokiński, A.; Sobów, T.; Kłoszewska, I.; Kostka, T. Mechanisms of the anorexia of aging—A review. Age 2015, 37. [CrossRef] [PubMed]
Bohannon, R.W. Minimal clinically important difference for grip strength: A systematic review. Soc. Phys. Ther. Sci. 2019, 31, 75–78. [CrossRef] [PubMed]
Beaudart, C.; Rolland, Y.; Cruz-Jentoft, A.J.; Bauer, J.M.; Sieber, C.; Cooper, C.; Al-Daghri, N.; Araujo de Carvalho, I.; Bautmans, I.; Bernabei, R.; et al. Assessment of Muscle Function and Physical Performance in Daily Clinical Practice: A position paper endorsed by the European Society for Clinical and Economic Aspects of Osteoporosis, Osteoarthritis and Musculoskeletal Diseases (ESCEO). Calcif. Tissue Int. 2019, 105, 1–14. [CrossRef] [PubMed]
Robinson, S.; Granic, A.; Sayer, A.A. Nutrition and muscle strength, as the key component of sarcopenia: An overview of current evidence. Nutrients 2019, 11, 2942. [CrossRef] [PubMed]
Úbeda, N.; Achón, M.; Varela-Moreiras, G. Omega 3 fatty acids in the elderly. Br. J. Nutr. 2012, 107, s131–s151. [CrossRef] [PubMed]
Lauretani, F.; Semba, R.D.; Bandinelli, S.; Dayhoff-Brannigan, M.; Giacomini, V.; Corsi, A.M.; Guralnik, J.M.; Ferrucci, L. Low Plasma Carotenoids and Skeletal Muscle Strength Decline Over 6 Years. J. Gerontol. 2008, 63, 376–383. [CrossRef]
Rondanelli, M.; Faliva, M.; Monteferrario, F.; Peroni, G.; Repaci, E.; Allieri, F.; Perna, S. Novel insights on nutrient management of sarcopenia in elderly. Biomed Res. Int. 2015, 2015. [CrossRef]
Dupont, J.; Dedeyne, L.; Dalle, S.; Koppo, K.; Gielen, E. The role of omega-3 in the prevention and treatment of sarcopenia. Aging Clin. Exp. Res. 2019, 31, 825–836. [CrossRef]
Houston, D.K.; Cesari, M.; Ferrucci, L.; Cherubini, A.; Maggio, D.; Bartali, B.; Johnson, M.A.; Schwartz, G.G.; Kritchevsky, S.B. Association Between Vitamin D Status and Physical Performance: The InCHIANTI Study. J. Gerontol. 2007, 62, 440–446. [CrossRef]
Remelli, F.; Vitali, A.; Zurlo, A.; Volpato, S. Vitamin D deficiency and sarcopenia in older persons. Nutrients 2019, 11, 2861. [CrossRef] [PubMed]
Shea, M.K.; Loeser, R.F.; Hsu, F.C.; Booth, S.L.; Nevitt, M.; Simonsick, E.M.; Strotmeyer, E.S.; Vermeer, C.; Kritchevsky, S.B. Vitamin K Status and Lower Extremity Function in Older Adults: The Health Aging and Body Composition Study. J. Gerontol. Ser. A Biol. Sci. Med. Sci. 2016, 71, 1348–1355. [CrossRef] [PubMed]
Azuma, K.; Inoue, S. Multiple modes of vitamin K actions in aging-related musculoskeletal disorders. Int. J. Mol. Sci. 2019, 20, 2844. [CrossRef] [PubMed]
Clausen Torben; Everts Maria Regulation of the Na,K-pump in skeletal muscle. Int. Soc. Nephrol. 1989, 35, 1–13.
McLeod, J.C.; Stokes, T.; Phillips, S.M. Resistance exercise training as a primary countermeasure to age-related chronic disease. Front. Physiol. 2019, 10. [CrossRef]
Deutz, N.E.P.; Bauer, J.M.; Barazzoni, R.; Biolo, G.; Boirie, Y.; Bosy-Westphal, A.; Cederholm, T.; Cruz-Jentoft, A.; Krznariç, Z.; Nair, K.S.; et al. Protein intake and exercise for optimal muscle function with aging: Recommendations from the ESPEN Expert Group. Clin. Nutr. 2014, 33, 929–936. [CrossRef]
Kamo, T.; Ishii, H.; Suzuki, K.; Nishida, Y. The impact of malnutrition on efficacy of resistance training in community-dwelling older adults. Physiother. Res. Int. 2019, 24. [CrossRef]
Nilsson, M.I.; Mikhail, A.; Lan, L.; Carlo, A.D.; Hamilton, B.; Barnard, K.; Hettinga, B.P.; Hatcher, E.; Tarnopolsky, M.G.; Nederveen, J.P.; et al. A five-ingredient nutritional supplement and home-based resistance exercise improve lean mass and strength in free-living elderly. Nutrients 2020, 12, 2391. [CrossRef]
Gropper, S.S.; Tappen, R.M.; Vieira, E.R. Differences In Nutritional And Physical Health Indicators Among Older African Americans, European Americans, And Hispanic Americans. J. Nutr. Gerontol. Geriatr. 2019, 38, 205–217. [CrossRef]
Du, K.; Goates, S.; Arensberg, M.B.; Pereira, S.; Gaillard, T. Prevalence of Sarcopenia and Sarcopenic Obesity Vary with Race/Ethnicity and Advancing Age. Divers. Equal. Health Care 2018, 15. [CrossRef]
Kalonji, E.; Sirot, V.; Noel, L.; Guerin, T.; Margaritis, I.; Leblanc, J.-C. Nutritional Risk Assessment of Eleven Minerals and Trace Elements: Prevalence of Inadequate and Excessive Intakes from the Second French Total Diet Study. Eur. J. Nutr. Food Saf. 2015, 5, 281–296. [CrossRef]
Agence nationale de sécurité sanitaire de l’alimentation, de l’environnement et du travail (ANSES) Avis de l’ANSES, Saisine n◦2012-SA-0142; 14 rue Pierre et Marie Curie, 94701 Maisons-Alfort Cedex. 2015. Available online: https://www.anses.fr/fr/system/files/NUT2012sa0142.pdf (accessed on 1 October 2020).
Carriquiry, A.L. Assessing the prevalence of nutrient inadequacy. Public Health Nutr. 1998, 2, 23–33. [CrossRef] [PubMed]
