The journal of nutrition, health & aging

, Volume 23, Issue 1, pp 27–34 | Cite as

Low Levels of Branched Chain Amino Acids, Eicosapentaenoic Acid and Micronutrients are Associated with Low Muscle Mass, Strength and Function in Community-Dwelling Older Adults

  • S. ter Borg
  • Y. C. LuikingEmail author
  • A. van Helvoort
  • Y. Boirie
  • J. M. G. A. Schols
  • C. P. G. M. de Groot



Sarcopenia, the age-related decrease in muscle mass and function can result in adverse health outcomes and subsequent loss of independence. Inadequate nutrition is an important contributor to the aetiology of sarcopenia, and dietary strategies are studied to prevent or delay this geriatric syndrome.


The present study investigated whether there is an association between biochemical nutrient status markers, muscle parameters and sarcopenia in community-dwelling older adults.


Data from the cross-sectional Maastricht Sarcopenia study (MaSS) were used, in which skeletal muscle index (SMI), 4 meter gait speed, 5 times chair stand and handgrip strength were assessed among older adults (n=227). Sarcopenia was defined following the algorithm of the European Working Group on Sarcopenia in Older People. Fasted blood samples were analyses on amino acids levels, RBC phospholipid profile, 25-hydroxyvitamin D (25(OH)D), α-tocopherol, magnesium and homocysteine were determined in fasted blood levels. Generalized linear modelling and logistic regression were used for data analysis.


Lower blood levels of essential amino acids (EAA), total branched-chain amino acids (BCAA) and leucine were associated with lower SMI (P<0.001), strength (P<0.001) and longer time to complete the chair stand (P<0.05), whereas no association was found for total amino acids (TAA). Lower levels of eicosapentaenoic acid (EPA), 25(OH)D and homocysteine were associated with lower muscle parameter values (P<0.05). No significant associations were found for SFA, MUFA, PUFA, n-3 and n-6 fatty acids, docosahexaenoic acid (DHA), α-tocopherol-cholesterol ratio and magnesium. Sarcopenia was more frequent among those with lower levels of leucine, BCAA, EAA, EPA, 25(OH)D and higher levels of homocysteine (P<0.05). Age and BMI were identified as relevant covariates. A robust association was only found for lower gait speed and lower 25(OH)D levels.


Compromised muscle parameters are associated with low blood values of specific amino acids, fatty acids, vitamin D and high homocysteine.

Key words

Sarcopenia older adults amino acids 25-hydroxyvitamin D n-3 fatty acids 


  1. 1.
    Koopman R, van Loon LJ. Aging, exercise, and muscle protein metabolism. Journal of applied physiology 2009;106: 2040–2048CrossRefGoogle Scholar
  2. 2.
    Short KR, Nair KS. Mechanisms of sarcopenia of aging. Journal of endocrinological investigation 1999;22: 95–105Google Scholar
  3. 3.
    Lindle RS, Metter EJ, Lynch NA et al. Age and gender comparisons of muscle strength in 654 women and men aged 20–93 yr. Journal of applied physiology 1997;83: 1581–1587CrossRefGoogle Scholar
  4. 4.
    Landi F, Calvani R, Cesari M et al. Sarcopenia: an overview on current definitions, diagnosis and treatment. Curr Protein Pept Sci, 2017Google Scholar
  5. 5.
    United Nations. Department of Economic and Social Affairs. Population Division Worlds Population Ageing: 1950–2050., accessed 16–07–2017.
  6. 6.
    Cruz–Jentoft AJ, Baeyens JP, Bauer JM et al. Sarcopenia: European consensus on definition and diagnosis: Report of the European Working Group on Sarcopenia in Older People. Age and ageing 2010;39: 412–423CrossRefGoogle Scholar
  7. 7.
    Morley JE, Argiles JM, Evans WJ et al. Nutritional recommendations for the management of sarcopenia. Journal of the American Medical Directors Association 2010;11: 391–396CrossRefGoogle Scholar
  8. 8.
    Bauer J, Biolo G, Cederholm T et al. Evidence–based recommendations for optimal dietary protein intake in older people: a position paper from the PROT–AGE Study Group. Journal of the American Medical Directors Association 2013;14: 542–559CrossRefGoogle Scholar
  9. 9.
    Verlaan S, Aspray TJ, Bauer JM et al. Nutritional status, body composition, and quality of life in community–dwelling sarcopenic and non–sarcopenic older adults: A case–control study. Clin Nutr 2017;36: 267–274CrossRefGoogle Scholar
  10. 10.
    Ten Borg S, de Groot LC, Mijnarends DM et al. Differences in Nutrient Intake and Biochemical Nutrient Status Between Sarcopenic and Nonsarcopenic Older Adults–Results From the Maastricht Sarcopenia Study. Journal of the American Medical Directors Association 2016;17: 393–401Google Scholar
  11. 11.
    Houston DK, Nicklas BJ, Ding J et al. Dietary protein intake is associated with lean mass change in older, community–dwelling adults: the Health, Aging, and Body Composition (Health ABC) Study. Am J Clin Nutr 2008;87: 150–155CrossRefGoogle Scholar
  12. 12.
    Houston DK, Tooze JA, Garcia K et al. Protein Intake and Mobility Limitation in Community–Dwelling Older Adults: the Health ABC Study. J Am Geriatr Soc 2017;65: 1705–1711CrossRefGoogle Scholar
  13. 13.
    McDonald CK, Ankarfeldt MZ, Capra S et al. Lean body mass change over 6 years is associated with dietary leucine intake in an older Danish population. The British journal of nutrition 2016;115: 1556–1562CrossRefGoogle Scholar
  14. 14.
    Mithal A, Bonjour JP, Boonen S et al. Impact of nutrition on muscle mass, strength, and performance in older adults. Osteoporosis international: a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA 2013;24: 1555–1566CrossRefGoogle Scholar
  15. 15.
    Robinson S, Cooper C, Aihie Sayer A. Nutrition and sarcopenia: a review of the evidence and implications for preventive strategies. Journal of aging research 2012;2012: 510801CrossRefGoogle Scholar
  16. 16.
    Sohl E, van Schoor NM, de Jongh RT et al. Vitamin D status is associated with functional limitations and functional decline in older individuals. The Journal of clinical endocrinology and metabolism 2013;98: E1483–1490CrossRefGoogle Scholar
  17. 17.
    Frison E, Boirie Y, Peuchant E et al. Plasma fatty acid biomarkers are associated with gait speed in community–dwelling older adults: The Three–City–Bordeaux study. Clin Nutr 2017;36: 416–422CrossRefGoogle Scholar
  18. 18.
    Boirie Y. Fighting sarcopenia in older frail subjects: protein fuel for strength, exercise for mass. Journal of the American Medical Directors Association 2013;14: 140–143CrossRefGoogle Scholar
  19. 19.
    Lips P. Vitamin D deficiency and secondary hyperparathyroidism in the elderly: consequences for bone loss and fractures and therapeutic implications. Endocrine reviews 2001;22: 477–501CrossRefGoogle Scholar
  20. 20.
    Brouwer–Brolsma EM, Vaes AM, van de Zwaluw NL et al. Relative importance of summer sun exposure, vitamin D intake, and genes to vitamin D status in Dutch older adults: The B–PROOF study. The Journal of steroid biochemistry and molecular biology 2016;164: 168–176Google Scholar
  21. 21.
    Mijnarends DM, Schols JM, Meijers JM et al. Instruments to assess sarcopenia and physical frailty in older people living in a community (care) setting: similarities and discrepancies. Journal of the American Medical Directors Association 2015;16: 301–308CrossRefGoogle Scholar
  22. 22.
    Janssen I, Heymsfield SB, Baumgartner RN et al. Estimation of skeletal muscle mass by bioelectrical impedance analysis. Journal of applied physiology 2000;89: 465–471CrossRefGoogle Scholar
  23. 23.
    Janssen I, Baumgartner RN, Ross R et al. Skeletal muscle cutpoints associated with elevated physical disability risk in older men and women. American journal of epidemiology 2004;159: 413–421CrossRefGoogle Scholar
  24. 24.
    Lauretani F, Russo CR, Bandinelli S et al. Age–associated changes in skeletal muscles and their effect on mobility: an operational diagnosis of sarcopenia. Journal of applied physiology 2003;95: 1851–1860CrossRefGoogle Scholar
  25. 25.
    Guralnik JM, Simonsick EM, Ferrucci L et al. A short physical performance battery assessing lower extremity function: association with self–reported disability and prediction of mortality and nursing home admission. Journal of gerontology 1994;49: M85–94Google Scholar
  26. 26.
    Terrlink T, van Leeuwen PA, Houdijk A. Plasma amino acids determined by liquid chromatography within 17 minutes. Clin Chem 1994;40: 245–249Google Scholar
  27. 27.
    Olia Araghi S, van Dijk SC, Ham AC et al. BMI and Body Fat Mass Is Inversely Associated with Vitamin D Levels in Older Individuals. The journal of nutrition, health & aging 2015;19: 980–985CrossRefGoogle Scholar
  28. 28.
    Sohl E, de Jongh RT, Swart KM et al. The association between vitamin D status and parameters for bone density and quality is modified by body mass index. Calcified tissue international 2015;96: 113–122Google Scholar
  29. 29.
    Elin RJ. Magnesium metabolism in health and disease. Disease–a–month: DM 1988;34: 161–218Google Scholar
  30. 30.
    Katsanos CS, Kobayashi H, Sheffield–Moore M et al. A high proportion of leucine is required for optimal stimulation of the rate of muscle protein synthesis by essential amino acids in the elderly. Am J Physiol Endocrinol Metab 2006;291: E381–387CrossRefGoogle Scholar
  31. 31.
    World Health Organization. Food and Agriculture Organization of the United Nations. United Nations University, 2007. Protein and amino acid requirements in human nutrition. Report of a joint FAO/WHO/UNU expert consultation (WHO Technical Report Series 935). World Health Organization.Google Scholar
  32. 32.
    Paddon–Jones D, Rasmussen BB. Dietary protein recommendations and the prevention of sarcopenia. Curr Opin Clin Nutr Metab Care 2009;12: 86–90CrossRefGoogle Scholar
  33. 33.
    Schmidt JA, Rinaldi S, Scalbert A et al. Plasma concentrations and intakes of amino acids in male meat–eaters, fish–eaters, vegetarians and vegans: a cross–sectional analysis in the EPIC–Oxford cohort. European journal of clinical nutrition 2016;70: 306–312CrossRefGoogle Scholar
  34. 34.
    Newgard CB, An J, Bain JR et al. A branched–chain amino acid–related metabolic signature that differentiates obese and lean humans and contributes to insulin resistance. Cell Metab 2009;9: 311–326CrossRefGoogle Scholar
  35. 35.
    Shah SH, Svetkey LP, Newgard CB. Branching out for detection of type 2 diabetes. Cell Metab 2011;13: 491–492CrossRefGoogle Scholar
  36. 36.
    Darmann and Cynober. Chapter 3: Approaches to study amino acid metabolism: from quantitative assays to flux assessment using stable isotopes. In: [Luc A Cynober, (ed)]] Metabolic and therapeutic aspects of amino acids in clinical nutrition, 2nd edition ed. CRC Press LLC, Washington DC, 2004Google Scholar
  37. 37.
    Abbatecola AM, Cherubini A, Guralnik JM et al. Plasma polyunsaturated fatty acids and age–related physical performance decline. Rejuvenation Res 2009;12: 25–32CrossRefGoogle Scholar
  38. 38.
    Ross AC, Manson JE, Abrams SA et al. The 2011 report on dietary reference intakes for calcium and vitamin D from the Institute of Medicine: what clinicians need to know. The Journal of clinical endocrinology and metabolism 2011;96: 53–58CrossRefGoogle Scholar
  39. 39.
    Wicherts IS, van Schoor NM, Boeke AJ et al. Vitamin D status predicts physical performance and its decline in older persons. The Journal of clinical endocrinology and metabolism 2007;92: 2058–2065Google Scholar
  40. 40.
    Tieland M, Brouwer E, Nienaber–Rousseau C et al. Compromised vitamin D status in frail elderly people is associated with reduced muscle mass and physical performance in “Dietary strategies to augment muscle mass in the elderly”. Dissertation, Wageningen University, 2013.Google Scholar
  41. 41.
    Kado DM, Bucur A, Selhub J et al. Homocysteine levels and decline in physical function: MacArthur Studies of Successful Aging. The American journal of medicine 2002;113: 537–542CrossRefGoogle Scholar
  42. 42.
    Swart KM, van Schoor NM, Heymans MW et al. Elevated homocysteine levels are associated with low muscle strength and functional limitations in older persons. The journal of nutrition, health & aging 2013;17: 578–584CrossRefGoogle Scholar
  43. 43.
    Weiss N, Keller C, Hoffmann U et al. Endothelial dysfunction and atherothrombosis in mild hyperhomocysteinemia. Vascular medicine 2002;7: 227–239CrossRefGoogle Scholar

Copyright information

© Serdi and Springer-Verlag France SAS, part of Springer Nature 2018

Authors and Affiliations

  • S. ter Borg
    • 1
  • Y. C. Luiking
    • 1
    • 2
    • 9
    Email author
  • A. van Helvoort
    • 1
    • 3
  • Y. Boirie
    • 4
    • 5
    • 6
  • J. M. G. A. Schols
    • 7
  • C. P. G. M. de Groot
    • 8
  1. 1.Danone Nutricia ResearchNutricia Advanced Medical NutritionUtrechtthe Netherlands
  2. 2.Center for Translational Research in Aging and Longevity, Department of Health and KinesiologyTexas A&M UniversityCollege StationUSA
  3. 3.NUTRIM, School of Nutrition and Translational Research in Metabolism, Faculty of Health, Medicine, and Life SciencesMaastricht UniversityMaastrichtThe Netherlands
  4. 4.University of Clermont Auvergne, Unité de Nutrition HumaineClermont-FerrandFrance
  5. 5.INRA, UMR 1019, UNHCRNH AuvergneClermont-FerrandFrance
  6. 6.CHU Clermont-Ferrand, Clinical Nutrition DepartmentClermont-FerrandFrance
  7. 7.Department of Health Services Research and Department of Family Medicine, School CAPHRIMaastricht UniversityMaastrichtthe Netherlands
  8. 8.Wageningen University, Division of Human NutritionWageningenthe Netherlands
  9. 9.Nutricia ResearchUtrechtthe Netherlands

Personalised recommendations