Impact of nutrition on muscle mass, strength, and performance in older adults

Osteoporosis International volume 24, pages1555–1566(2013)Cite this article

An Erratum to this article is available

Abstract

Muscle strength plays an important role in determining risk for falls, which result in fractures and other injuries. While bone loss has long been recognized as an inevitable consequence of aging, sarcopenia—the gradual loss of skeletal muscle mass and strength that occurs with advancing age—has recently received increased attention. A review of the literature was undertaken to identify nutritional factors that contribute to loss of muscle mass. The role of protein, acid–base balance, vitamin D/calcium, and other minor nutrients like B vitamins was reviewed. Muscle wasting is a multifactorial process involving intrinsic and extrinsic alterations. A loss of fast twitch fibers, glycation of proteins, and insulin resistance may play an important role in the loss of muscle strength and development of sarcopenia. Protein intake plays an integral part in muscle health and an intake of 1.0–1.2 g/kg of body weight per day is probably optimal for older adults. There is a moderate inverse relationship between vitamin D status and muscle strength. Chronic ingestion of acid-producing diets appears to have a negative impact on muscle performance, and decreases in vitamin B12 and folic acid intake may also impair muscle function through their action on homocysteine. An adequate nutritional intake and an optimal dietary acid–base balance are important elements of any strategy to preserve muscle mass and strength during aging.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

US$ 39.95

Tax calculation will be finalised during checkout.

Fig. 1

References

  1. 1.

    Rosenberg IH (1989) Epidemiologic and methodologic problems in determining nutritional status of older persons. Proceedings of a conference. Albuquerque, New Mexico, October 19–21, 1988. Am J Clin Nutr 50:1121–1235

    Google Scholar 

  2. 2.

    Baumgartner RN, Koehler KM, Gallagher D, Romero L, Heymsfield SB, Ross RR, Garry PJ, Lindeman RD (1998) Epidemiology of sarcopenia among the elderly in New Mexico. Am J Epidemiol 147:755–763

    PubMed  CAS  Article  Google Scholar 

  3. 3.

    Pichard C, Kyle UG, Bracco D, Slosman DO, Morabia A, Schutz Y (2000) Reference values of fat-free and fat masses by bioelectrical impedance analysis in 3393 healthy subjects. Nutrition 16:245–254

    PubMed  CAS  Article  Google Scholar 

  4. 4.

    Cruz-Jentoft AJ, Baeyens JP, Bauer JM et al (2010) Sarcopenia: European consensus on definition and diagnosis: report of the European Working Group on sarcopenia in older people. Age Ageing 39:412–423

    PubMed  Article  Google Scholar 

  5. 5.

    Castillo EM, Goodman-Gruen D, Kritz-Silverstein D, Morton DJ, Wingard DL, Barrett-Connor E (2003) Sarcopenia in elderly men and women: the Rancho Bernardo study. Am J Prev Med 25:226–231

    PubMed  Article  Google Scholar 

  6. 6.

    Janssen I (2006) Influence of sarcopenia on the development of physical disability: the Cardiovascular Health Study. J Am Geriatr Soc 54:56–62

    PubMed  Article  Google Scholar 

  7. 7.

    Janssen I, Heymsfield SB, Ross R (2002) Low relative skeletal muscle mass (sarcopenia) in older persons is associated with functional impairment and physical disability. J Am Geriatr Soc 50:889–896

    PubMed  Article  Google Scholar 

  8. 8.

    Lauretani F, Russo CR, Bandinelli S, Bartali B, Cavazzini C, Di Iorio A, Corsi AM, Rantanen T, Guralnik JM, Ferrucci L (2003) Age-associated changes in skeletal muscles and their effect on mobility: an operational diagnosis of sarcopenia. J Appl Physiol 95:1851–1860

    PubMed  Google Scholar 

  9. 9.

    Rolland Y, Lauwers-Cances V, Cournot M, Nourhashemi F, Reynish W, Riviere D, Vellas B, Grandjean H (2003) Sarcopenia, calf circumference, and physical function of elderly women: a cross-study. J Am Geriatr Soc 51:1120–1124

    PubMed  Article  Google Scholar 

  10. 10.

    Dutta C, Hadley EC (1995) The significance of sarcopenia in old age. J Gerontol A Biol Sci Med Sci 50 Spec No:1–4

    Google Scholar 

  11. 11.

    Thomas DR (2010) Sarcopenia. Clin Geriatr Med 26:331–346

    PubMed  Article  Google Scholar 

  12. 12.

    Di Monaco M, Vallero F, Di Monaco R, Tappero R (2011) Prevalence of sarcopenia and its association with osteoporosis in 313 older women following a hip fracture. Arch Gerontol Geriatr 52:71–74

    PubMed  Article  Google Scholar 

  13. 13.

    Fiatarone Singh MA, Singh NA, Hansen RD et al (2009) Methodology and baseline characteristics for the Sarcopenia and Hip Fracture study: a 5-year prospective study. J Gerontol A Biol Sci Med Sci 64:568–574

    PubMed  Article  Google Scholar 

  14. 14.

    Lang T, Cauley JA, Tylavsky F, Bauer D, Cummings S, Harris TB (2010) Computed tomographic measurements of thigh muscle cross-sectional area and attenuation coefficient predict hip fracture: the health, aging, and body composition study. J Bone Miner Res 25:513–519

    PubMed  Article  Google Scholar 

  15. 15.

    Boirie Y (2009) Physiopathological mechanism of sarcopenia. J Nutr Health Aging 13:717–723

    PubMed  CAS  Article  Google Scholar 

  16. 16.

    Katsanos CS, Kobayashi H, Sheffield-Moore M, Aarsland A, Wolfe RR (2005) Aging is associated with diminished accretion of muscle proteins after the ingestion of a small bolus of essential amino acids. Am J Clin Nutr 82:1065–1073

    PubMed  CAS  Google Scholar 

  17. 17.

    Volpi E, Mittendorfer B, Rasmussen BB, Wolfe RR (2000) The response of muscle protein anabolism to combined hyperaminoacidemia and glucose-induced hyperinsulinemia is impaired in the elderly. J Clin Endocrinol Metab 85:4481–4490

    PubMed  CAS  Article  Google Scholar 

  18. 18.

    Fulgoni VL 3rd (2008) Current protein intake in America: analysis of the National Health and Nutrition Examination Survey, 2003–2004. Am J Clin Nutr 87:1554S–1557S

    PubMed  CAS  Google Scholar 

  19. 19.

    Kerstetter JE, O'Brien KO, Insogna KL (2003) Low protein intake: the impact on calcium and bone homeostasis in humans. J Nutr 133:855S–861S

    PubMed  CAS  Google Scholar 

  20. 20.

    Houston DK, Nicklas BJ, Ding J, Harris TB, Tylavsky FA, Newman AB, Lee JS, Sahyoun NR, Visser M, Kritchevsky SB (2008) 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 87:150–155

    PubMed  CAS  Google Scholar 

  21. 21.

    Gaffney-Stomberg E, Insogna KL, Rodriguez NR, Kerstetter JE (2009) Increasing dietary protein requirements in elderly people for optimal muscle and bone health. J Am Geriatr Soc 57:1073–1079

    PubMed  Article  Google Scholar 

  22. 22.

    Campbell WW, Leidy HJ (2007) Dietary protein and resistance training effects on muscle and body composition in older persons. J Am Coll Nutr 26:696S–703S

    PubMed  CAS  Google Scholar 

  23. 23.

    Schurch MA, Rizzoli R, Slosman D, Vadas L, Vergnaud P, Bonjour JP (1998) Protein supplements increase serum insulin-like growth factor-I levels and attenuate proximal femur bone loss in patients with recent hip fracture. A randomized, double-blind, placebo-controlled trial. Ann Intern Med 128:801–809

    PubMed  CAS  Article  Google Scholar 

  24. 24.

    Andrews RD, MacLean DA, Riechman SE (2006) Protein intake for skeletal muscle hypertrophy with resistance training in seniors. Int J Sport Nutr Exerc Metab 16:362–372

    PubMed  CAS  Google Scholar 

  25. 25.

    Bemben MG, Witten MS, Carter JM, Eliot KA, Knehans AW, Bemben DA (2010) The effects of supplementation with creatine and protein on muscle strength following a traditional resistance training program in middle-aged and older men. J Nutr Health Aging 14:155–159

    PubMed  CAS  Article  Google Scholar 

  26. 26.

    Candow DG, Chilibeck PD, Facci M, Abeysekara S, Zello GA (2006) Protein supplementation before and after resistance training in older men. Eur J Appl Physiol 97:548–556

    PubMed  CAS  Article  Google Scholar 

  27. 27.

    Eliot KA, Knehans AW, Bemben DA, Witten MS, Carter J, Bemben MG (2008) The effects of creatine and whey protein supplementation on body composition in men aged 48 to 72 years during resistance training. J Nutr Health Aging 12:208–212

    PubMed  CAS  Article  Google Scholar 

  28. 28.

    Holm L, Olesen JL, Matsumoto K, Doi T, Mizuno M, Alsted TJ, Mackey AL, Schwarz P, Kjaer M (2008) Protein-containing nutrient supplementation following strength training enhances the effect on muscle mass, strength, and bone formation in postmenopausal women. J Appl Physiol 105:274–281

    PubMed  CAS  Article  Google Scholar 

  29. 29.

    Dillon EL, Sheffield-Moore M, Paddon-Jones D, Gilkison C, Sanford AP, Casperson SL, Jiang J, Chinkes DL, Urban RJ (2009) Amino acid supplementation increases lean body mass, basal muscle protein synthesis, and insulin-like growth factor-I expression in older women. J Clin Endocrinol Metab 94:1630–1637

    PubMed  CAS  Article  Google Scholar 

  30. 30.

    Ferrando AA, Paddon-Jones D, Hays NP, Kortebein P, Ronsen O, Williams RH, McComb A, Symons TB, Wolfe RR, Evans W (2010) EAA supplementation to increase nitrogen intake improves muscle function during bed rest in the elderly. Clin Nutr 29:18–23

    PubMed  CAS  Article  Google Scholar 

  31. 31.

    Onambele-Pearson GL, Breen L, Stewart CE (2010) Influences of carbohydrate plus amino acid supplementation on differing exercise intensity adaptations in older persons: skeletal muscle and endocrine responses. Age (Dordr) 32:125–138

    CAS  Article  Google Scholar 

  32. 32.

    Solerte SB, Gazzaruso C, Bonacasa R, Rondanelli M, Zamboni M, Basso C, Locatelli E, Schifino N, Giustina A, Fioravanti M (2008) Nutritional supplements with oral amino acid mixtures increases whole-body lean mass and insulin sensitivity in elderly subjects with sarcopenia. Am J Cardiol 101:69E–77E

    PubMed  CAS  Article  Google Scholar 

  33. 33.

    Koopman R, van Loon LJ (2009) Aging, exercise, and muscle protein metabolism. J Appl Physiol 106:2040–2048

    PubMed  CAS  Article  Google Scholar 

  34. 34.

    Blomstrand E, Eliasson J, Karlsson HK, Kohnke R (2006) Branched-chain amino acids activate key enzymes in protein synthesis after physical exercise. J Nutr 136:269S–273S

    PubMed  CAS  Google Scholar 

  35. 35.

    Clemmons DR (2009) Role of IGF-I in skeletal muscle mass maintenance. Trends Endocrinol Metab 20:349–356

    PubMed  CAS  Article  Google Scholar 

  36. 36.

    Fujita S, Volpi E (2006) Amino acids and muscle loss with aging. J Nutr 136:277S–280S

    PubMed  CAS  Google Scholar 

  37. 37.

    Kim JS, Wilson JM, Lee SR (2010) Dietary implications on mechanisms of sarcopenia: roles of protein, amino acids and antioxidants. J Nutr Biochem 21:1–13

    PubMed  Article  CAS  Google Scholar 

  38. 38.

    Kimball SR, Jefferson LS (2006) Signaling pathways and molecular mechanisms through which branched-chain amino acids mediate translational control of protein synthesis. J Nutr 136:227S–231S

    PubMed  CAS  Google Scholar 

  39. 39.

    Millward DJ, Layman DK, Tome D, Schaafsma G (2008) Protein quality assessment: impact of expanding understanding of protein and amino acid needs for optimal health. Am J Clin Nutr 87:1576S–1581S

    PubMed  CAS  Google Scholar 

  40. 40.

    Paddon-Jones D, Rasmussen BB (2009) Dietary protein recommendations and the prevention of sarcopenia. Curr Opin Clin Nutr Metab Care 12:86–90

    PubMed  CAS  Article  Google Scholar 

  41. 41.

    Rennie MJ, Bohe J, Smith K, Wackerhage H, Greenhaff P (2006) Branched-chain amino acids as fuels and anabolic signals in human muscle. J Nutr 136:264S–268S

    PubMed  CAS  Google Scholar 

  42. 42.

    Verdijk LB, Jonkers RA, Gleeson BG, Beelen M, Meijer K, Savelberg HH, Wodzig WK, Dendale P, van Loon LJ (2009) Protein supplementation before and after exercise does not further augment skeletal muscle hypertrophy after resistance training in elderly men. Am J Clin Nutr 89:608–616

    PubMed  CAS  Article  Google Scholar 

  43. 43.

    Rand WM, Pellett PL, Young VR (2003) Meta-analysis of nitrogen balance studies for estimating protein requirements in healthy adults. Am J Clin Nutr 77:109–127

    PubMed  CAS  Google Scholar 

  44. 44.

    Wolfe RR (2008) Protein Summit: consensus areas and future research. Am J Clin Nutr 87:1582S–1583S

    PubMed  CAS  Google Scholar 

  45. 45.

    Rodriguez NR, Garlick PJ (2008) Introduction to Protein Summit 2007: exploring the impact of high-quality protein on optimal health. Am J Clin Nutr 87:1551S–1553S

    PubMed  CAS  Google Scholar 

  46. 46.

    Martin WF, Armstrong LE, Rodriguez NR (2005) Dietary protein intake and renal function. Nutr Metab (Lond) 2:25

    Article  CAS  Google Scholar 

  47. 47.

    Kovesdy CP, Kalantar-Zadeh K (2009) Why is protein-energy wasting associated with mortality in chronic kidney disease? Semin Nephrol 29:3–14

    PubMed  CAS  Article  Google Scholar 

  48. 48.

    Ceglia L (2011) Vitamin D and skeletal muscle function. In: Feldman D, Wesley Pike J, Adams JS (eds) Vitamin D. Academic, London, pp 2023–2042

    Google Scholar 

  49. 49.

    Bischoff-Ferrari HA, Borchers M, Gudat F, Durmuller U, Stahelin HB, Dick W (2004) Vitamin D receptor expression in human muscle tissue decreases with age. J Bone Miner Res 19:265–269

    PubMed  CAS  Article  Google Scholar 

  50. 50.

    Wang Y, DeLuca HF (2011) Is the vitamin d receptor found in muscle? Endocrinology 152:354–363

    PubMed  CAS  Article  Google Scholar 

  51. 51.

    Garcia LA, King KK, Ferrini MG, Norris KC, Artaza JN (2011) 1,25(OH)2vitamin D3 stimulates myogenic differentiation by inhibiting cell proliferation and modulating the expression of promyogenic growth factors and myostatin in C2C12 skeletal muscle cells. Endocrinology 152:2976–2986

    PubMed  CAS  Article  Google Scholar 

  52. 52.

    Annweiler C, Montero-Odasso M, Schott AM, Berrut G, Fantino B, Beauchet O (2010) Fall prevention and vitamin D in the elderly: an overview of the key role of the non-bone effects. J Neuroeng Rehabil 7:50

    PubMed  Article  Google Scholar 

  53. 53.

    Bischoff-Ferrari HA, Dietrich T, Orav EJ, Hu FB, Zhang Y, Karlson EW, Dawson-Hughes B (2004) Higher 25-hydroxyvitamin D concentrations are associated with better lower-extremity function in both active and inactive persons aged > or =60 y. Am J Clin Nutr 80:752–758

    PubMed  CAS  Google Scholar 

  54. 54.

    Wicherts IS, van Schoor NM, Boeke AJ, Visser M, Deeg DJ, Smit J, Knol DL, Lips P (2007) Vitamin D status predicts physical performance and its decline in older persons. J Clin Endocrinol Metab 92:2058–2065

    PubMed  CAS  Article  Google Scholar 

  55. 55.

    Dam TT, von Muhlen D, Barrett-Connor EL (2009) Sex-specific association of serum vitamin D levels with physical function in older adults. Osteoporos Int 20:751–760

    PubMed  CAS  Article  Google Scholar 

  56. 56.

    Gerdhem P, Ivaska KK, Isaksson A, Pettersson K, Vaananen HK, Obrant KJ, Akesson K (2007) Associations between homocysteine, bone turnover, BMD, mortality, and fracture risk in elderly women. J Bone Miner Res 22:127–134

    PubMed  CAS  Article  Google Scholar 

  57. 57.

    Foo LH, Zhang Q, Zhu K, Ma G, Hu X, Greenfield H, Fraser DR (2009) Low vitamin D status has an adverse influence on bone mass, bone turnover, and muscle strength in Chinese adolescent girls. J Nutr 139:1002–1007

    PubMed  CAS  Article  Google Scholar 

  58. 58.

    Ward KA, Das G, Berry JL, Roberts SA, Rawer R, Adams JE, Mughal Z (2009) Vitamin D status and muscle function in post-menarchal adolescent girls. J Clin Endocrinol Metab 94:559–563

    PubMed  CAS  Article  Google Scholar 

  59. 59.

    Pfeifer M, Begerow B, Minne HW, Schlotthauer T, Pospeschill M, Scholz M, Lazarescu AD, Pollahne W (2001) Vitamin D status, trunk muscle strength, body sway, falls, and fractures among 237 postmenopausal women with osteoporosis. Exp Clin Endocrinol Diabetes 109:87–92

    PubMed  CAS  Article  Google Scholar 

  60. 60.

    Kuchuk NO, Pluijm SM, van Schoor NM, Looman CW, Smit JH, Lips P (2009) Relationships of serum 25-hydroxyvitamin D to bone mineral density and serum parathyroid hormone and markers of bone turnover in older persons. J Clin Endocrinol Metab 94:1244–1250

    PubMed  Article  CAS  Google Scholar 

  61. 61.

    Marantes I, Achenbach SJ, Atkinson EJ, Khosla S, Melton LJ 3rd, Amin S (2011) Is vitamin D a determinant of muscle mass and strength? J Bone Miner Res 26:2860–2871

    PubMed  CAS  Article  Google Scholar 

  62. 62.

    Glerup H, Mikkelsen K, Poulsen L, Hass E, Overbeck S, Andersen H, Charles P, Eriksen EF (2000) Hypovitaminosis D myopathy without biochemical signs of osteomalacic bone involvement. Calcif Tissue Int 66:419–424

    PubMed  CAS  Article  Google Scholar 

  63. 63.

    Pfeifer M, Begerow B, Minne HW, Abrams C, Nachtigall D, Hansen C (2000) Effects of a short-term vitamin D and calcium supplementation on body sway and secondary hyperparathyroidism in elderly women. J Bone Miner Res 15:1113–1118

    PubMed  CAS  Article  Google Scholar 

  64. 64.

    Latham NK, Anderson CS, Lee A, Bennett DA, Moseley A, Cameron ID (2003) A randomized, controlled trial of quadriceps resistance exercise and vitamin D in frail older people: the Frailty Interventions Trial in Elderly Subjects (FITNESS). J Am Geriatr Soc 51:291–299

    PubMed  Article  Google Scholar 

  65. 65.

    Kenny AM, Biskup B, Robbins B, Marcella G, Burleson JA (2003) Effects of vitamin D supplementation on strength, physical function, and health perception in older, community-dwelling men. J Am Geriatr Soc 51:1762–1767

    PubMed  Article  Google Scholar 

  66. 66.

    El-Hajj Fuleihan G, Nabulsi M, Tamim H, Maalouf J, Salamoun M, Khalife H, Choucair M, Arabi A, Vieth R (2006) Effect of vitamin D replacement on musculoskeletal parameters in school children: a randomized controlled trial. J Clin Endocrinol Metab 91:405–412

    PubMed  Article  CAS  Google Scholar 

  67. 67.

    Pfeifer M, Begerow B, Minne HW, Suppan K, Fahrleitner-Pammer A, Dobnig H (2009) Effects of a long-term vitamin D and calcium supplementation on falls and parameters of muscle function in community-dwelling older individuals. Osteoporos Int 20:315–322

    PubMed  CAS  Article  Google Scholar 

  68. 68.

    Ward KA, Das G, Roberts SA, Berry JL, Adams JE, Rawer R, Mughal MZ (2010) A randomized, controlled trial of vitamin D supplementation upon musculoskeletal health in postmenarchal females. J Clin Endocrinol Metab 95:4643–4651

    PubMed  CAS  Article  Google Scholar 

  69. 69.

    Lips P, Binkley N, Pfeifer M, Recker R, Samanta S, Cohn DA, Chandler J, Rosenberg E, Papanicolaou DA (2010) Once-weekly dose of 8400 IU vitamin D(3) compared with placebo: effects on neuromuscular function and tolerability in older adults with vitamin D insufficiency. Am J Clin Nutr 91:985–991

    PubMed  CAS  Article  Google Scholar 

  70. 70.

    Verschueren SM, Bogaerts A, Delecluse C, Claessens AL, Haentjens P, Vanderschueren D, Boonen S (2011) The effects of whole-body vibration training and vitamin D supplementation on muscle strength, muscle mass, and bone density in institutionalized elderly women: a 6-month randomized, controlled trial. J Bone Miner Res 26:42–49

    PubMed  CAS  Article  Google Scholar 

  71. 71.

    Bischoff-Ferrari HA, Dawson-Hughes B, Willett WC, Staehelin HB, Bazemore MG, Zee RY, Wong JB (2004) Effect of vitamin D on falls: a meta-analysis. JAMA 291:1999–2006

    PubMed  CAS  Article  Google Scholar 

  72. 72.

    Sorensen OH, Lund B, Saltin B, Andersen RB, Hjorth L, Melsen F, Mosekilde L (1979) Myopathy in bone loss of ageing: improvement by treatment with 1 alpha-hydroxycholecalciferol and calcium. Clin Sci (Lond) 56:157–161

    CAS  Google Scholar 

  73. 73.

    Sato Y, Iwamoto J, Kanoko T, Satoh K (2005) Low-dose vitamin D prevents muscular atrophy and reduces falls and hip fractures in women after stroke: a randomized controlled trial. Cerebrovasc Dis 20:187–192

    PubMed  CAS  Article  Google Scholar 

  74. 74.

    McLean RR, Jacques PF, Selhub J, Tucker KL, Samelson EJ, Broe KE, Hannan MT, Cupples LA, Kiel DP (2004) Homocysteine as a predictive factor for hip fracture in older persons. N Engl J Med 350:2042–2049

    PubMed  CAS  Article  Google Scholar 

  75. 75.

    van Meurs JB, Dhonukshe-Rutten RA, Pluijm SM et al (2004) Homocysteine levels and the risk of osteoporotic fracture. N Engl J Med 350:2033–2041

    PubMed  Article  Google Scholar 

  76. 76.

    Kado DM, Bucur A, Selhub J, Rowe JW, Seeman T (2002) Homocysteine levels and decline in physical function: MacArthur Studies of Successful Aging. Am J Med 113:537–542

    PubMed  CAS  Article  Google Scholar 

  77. 77.

    Kuo HK, Liao KC, Leveille SG, Bean JF, Yen CJ, Chen JH, Yu YH, Tai TY (2007) Relationship of homocysteine levels to quadriceps strength, gait speed, and late-life disability in older adults. J Gerontol A Biol Sci Med Sci 62:434–439

    PubMed  Article  Google Scholar 

  78. 78.

    McDermott MM, Ferrucci L, Guralnik JM et al (2007) Elevated levels of inflammation, d-dimer, and homocysteine are associated with adverse calf muscle characteristics and reduced calf strength in peripheral arterial disease. J Am Coll Cardiol 50:897–905

    PubMed  CAS  Article  Google Scholar 

  79. 79.

    Sato Y, Honda Y, Iwamoto J, Kanoko T, Satoh K (2005) Effect of folate and mecobalamin on hip fractures in patients with stroke: a randomized controlled trial. JAMA 293:1082–1088

    PubMed  CAS  Article  Google Scholar 

  80. 80.

    Bailey JL, England BK, Long RC, Mitch WE (1996) Influence of acid loading, extracellular pH and uremia on intracellular pH in muscle. Miner Electrolyte Metab 22:66–68

    PubMed  CAS  Google Scholar 

  81. 81.

    Frassetto LA, Morris RC Jr, Sebastian A (1996) Effect of age on blood acid-base composition in adult humans: role of age-related renal functional decline. Am J Physiol 271:F1114–F1122

    PubMed  CAS  Google Scholar 

  82. 82.

    Green J, Kleeman CR (1991) Role of bone in regulation of systemic acid-base balance. Kidney Int 39:9–26

    PubMed  CAS  Article  Google Scholar 

  83. 83.

    Cahill GF Jr (1970) Starvation in man. N Engl J Med 282:668–675

    PubMed  CAS  Article  Google Scholar 

  84. 84.

    Askanazi J, Carpentier YA, Michelsen CB, Elwyn DH, Furst P, Kantrowitz LR, Gump FE, Kinney JM (1980) Muscle and plasma amino acids following injury. Influence of intercurrent infection. Ann Surg 192:78–85

    PubMed  CAS  Article  Google Scholar 

  85. 85.

    Aulick LH, Wilmore DW (1979) Increased peripheral amino acid release following burn injury. Surgery 85:560–565

    PubMed  CAS  Google Scholar 

  86. 86.

    Souba WW, Smith RJ, Wilmore DW (1985) Glutamine metabolism by the intestinal tract. JPEN J Parenter Enter Nutr 9:608–617

    CAS  Article  Google Scholar 

  87. 87.

    Williamson DH (1980) Muscle protein degradation and amino acid metabolism in human injury. Biochem Soc Trans 8:497

    PubMed  CAS  Google Scholar 

  88. 88.

    Garibotto G, Deferrari G, Robaudo C, Saffioti S, Sofia A, Russo R, Tizianello A (1995) Disposal of exogenous amino acids by muscle in patients with chronic renal failure. Am J Clin Nutr 62:136–142

    PubMed  CAS  Google Scholar 

  89. 89.

    Vazquez JA, Adibi SA (1992) Protein sparing during treatment of obesity: ketogenic versus nonketogenic very low calorie diet. Metabolism 41:406–414

    PubMed  CAS  Article  Google Scholar 

  90. 90.

    Papadoyannakis NJ, Stefanidis CJ, McGeown M (1984) The effect of the correction of metabolic acidosis on nitrogen and potassium balance of patients with chronic renal failure. Am J Clin Nutr 40:623–627

    PubMed  CAS  Google Scholar 

  91. 91.

    Gougeon-Reyburn R, Lariviere F, Marliss EB (1991) Effects of bicarbonate supplementation on urinary mineral excretion during very low energy diets. Am J Med Sci 302:67–74

    PubMed  CAS  Article  Google Scholar 

  92. 92.

    Williams B, Layward E, Walls J (1991) Skeletal muscle degradation and nitrogen wasting in rats with chronic metabolic acidosis. Clin Sci (Lond) 80:457–462

    CAS  Google Scholar 

  93. 93.

    May RC, Kelly RA, Mitch WE (1986) Metabolic acidosis stimulates protein degradation in rat muscle by a glucocorticoid-dependent mechanism. J Clin Invest 77:614–621

    PubMed  CAS  Article  Google Scholar 

  94. 94.

    Owen EE, Robinson RR (1963) Amino acid extraction and ammonia metabolism by the human kidney during the prolonged administration of ammonium chloride. J Clin Invest 42:263–276

    PubMed  CAS  Article  Google Scholar 

  95. 95.

    Price SR, Du JD, Bailey JL, Mitch WE (2001) Molecular mechanisms regulating protein turnover in muscle. Am J Kidney Dis 37:S112–S114

    PubMed  CAS  Article  Google Scholar 

  96. 96.

    Ballmer PE, McNurlan MA, Hulter HN, Anderson SE, Garlick PJ, Krapf R (1995) Chronic metabolic acidosis decreases albumin synthesis and induces negative nitrogen balance in humans. J Clin Invest 95:39–45

    PubMed  CAS  Article  Google Scholar 

  97. 97.

    Dawson-Hughes B, Harris SS, Ceglia L (2008) Alkaline diets favor lean tissue mass in older adults. Am J Clin Nutr 87:662–665

    PubMed  CAS  Google Scholar 

  98. 98.

    Ceglia L, Harris SS, Abrams SA, Rasmussen HM, Dallal GE, Dawson-Hughes B (2009) Potassium bicarbonate attenuates the urinary nitrogen excretion that accompanies an increase in dietary protein and may promote calcium absorption. J Clin Endocrinol Metab 94:645–653

    PubMed  CAS  Article  Google Scholar 

  99. 99.

    Dawson-Hughes B, Harris SS, Palermo NJ, Castaneda-Sceppa C, Rasmussen HM, Dallal GE (2009) Treatment with potassium bicarbonate lowers calcium excretion and bone resorption in older men and women. J Clin Endocrinol Metab 94:96–102

    PubMed  CAS  Article  Google Scholar 

  100. 100.

    Frassetto L, Morris RC Jr, Sebastian A (1997) Potassium bicarbonate reduces urinary nitrogen excretion in postmenopausal women. J Clin Endocrinol Metab 82:254–259

    PubMed  CAS  Article  Google Scholar 

  101. 101.

    Vieth R, Fraser D (1979) Kinetic behavior of 25-hydroxyvitamin D-1-hydroxylase and -24-hydroxylase in rat kidney mitochondria. J Biol Chem 254:12455–12460

    PubMed  CAS  Google Scholar 

  102. 102.

    Langman CB, Bushinsky DA, Favus MJ, Coe FL (1986) Ca and P regulation of 1,25(OH)2D3 synthesis by vitamin D-replete rat tubules during acidosis. Am J Physiol 251:F911–F918

    PubMed  CAS  Google Scholar 

  103. 103.

    Krapf R, Vetsch R, Vetsch W, Hulter HN (1992) Chronic metabolic acidosis increases the serum concentration of 1,25-dihydroxyvitamin D in humans by stimulating its production rate. Critical role of acidosis-induced renal hypophosphatemia. J Clin Invest 90:2456–2463

    PubMed  CAS  Article  Google Scholar 

  104. 104.

    Mizwicki MT, Bishop JE, Norman AW (2005) Applications of the vitamin D sterol-vitamin D receptor (VDR) conformational ensemble model. Steroids 70:464–471

    PubMed  CAS  Article  Google Scholar 

  105. 105.

    Hulter HN (1985) Effects and interrelationships of PTH, Ca2+, vitamin D, and Pi in acid-base homeostasis. Am J Physiol 248:F739–F752

    PubMed  CAS  Google Scholar 

  106. 106.

    Hulter HN, Halloran BP, Toto RD, Peterson JC (1985) Long-term control of plasma calcitriol concentration in dogs and humans. Dominant role of plasma calcium concentration in experimental hyperparathyroidism. J Clin Invest 76:695–702

    PubMed  CAS  Article  Google Scholar 

  107. 107.

    Dawson-Hughes B, Castaneda-Sceppa C, Harris SS, Palermo NJ, Cloutier G, Ceglia L, Dallal GE (2010) Impact of supplementation with bicarbonate on lower-extremity muscle performance in older men and women. Osteoporos Int 21:1171–1179

    PubMed  CAS  Article  Google Scholar 

  108. 108.

    Roth DA, Brooks GA (1990) Lactate and pyruvate transport is dominated by a pH gradient-sensitive carrier in rat skeletal muscle sarcolemmal vesicles. Arch Biochem Biophys 279:386–394

    PubMed  CAS  Article  Google Scholar 

  109. 109.

    Mainwood GW, Renaud JM (1985) The effect of acid-base balance on fatigue of skeletal muscle. Can J Physiol Pharmacol 63:403–416

    PubMed  CAS  Article  Google Scholar 

  110. 110.

    Verbitsky O, Mizrahi J, Levin M, Isakov E (1997) Effect of ingested sodium bicarbonate on muscle force, fatigue, and recovery. J Appl Physiol 83:333–337

    PubMed  CAS  Google Scholar 

  111. 111.

    Price M, Moss P, Rance S (2003) Effects of sodium bicarbonate ingestion on prolonged intermittent exercise. Med Sci Sports Exerc 35:1303–1308

    PubMed  CAS  Article  Google Scholar 

  112. 112.

    Horswill CA, Costill DL, Fink WJ, Flynn MG, Kirwan JP, Mitchell JB, Houmard JA (1988) Influence of sodium bicarbonate on sprint performance: relationship to dosage. Med Sci Sports Exerc 20:566–569

    PubMed  CAS  Google Scholar 

  113. 113.

    McCartney N, Heigenhauser GJ, Jones NL (1983) Effects of pH on maximal power output and fatigue during short-term dynamic exercise. J Appl Physiol 55:225–229

    PubMed  CAS  Google Scholar 

  114. 114.

    Webster MJ, Webster MN, Crawford RE, Gladden LB (1993) Effect of sodium bicarbonate ingestion on exhaustive resistance exercise performance. Med Sci Sports Exerc 25:960–965

    PubMed  CAS  Google Scholar 

  115. 115.

    Lee WJ (2011) IGF-I exerts an anti-inflammatory effect on skeletal muscle cells through down-regulation of TLR4 signaling. Immune Netw 11:223–226

    PubMed  Article  Google Scholar 

  116. 116.

    Biolo G, Tipton KD, Klein S, Wolfe RR (1997) An abundant supply of amino acids enhances the metabolic effect of exercise on muscle protein. Am J Physiol 273:E122–E129

    PubMed  CAS  Google Scholar 

  117. 117.

    Dickinson JM, Fry CS, Drummond MJ, Gundermann DM, Walker DK, Glynn EL, Timmerman KL, Dhanani S, Volpi E, Rasmussen BB (2011) Mammalian target of rapamycin complex 1 activation is required for the stimulation of human skeletal muscle protein synthesis by essential amino acids. J Nutr 141:856–862

    PubMed  CAS  Article  Google Scholar 

  118. 118.

    Farnfield MM, Breen L, Carey KA, Garnham A, Cameron-Smith D (2012) Activation of mTOR signalling in young and old human skeletal muscle in response to combined resistance exercise and whey protein ingestion. Appl Physiol Nutr Metab 37:21–30

    PubMed  CAS  Article  Google Scholar 

  119. 119.

    Moore DR, Atherton PJ, Rennie MJ, Tarnopolsky MA, Phillips SM (2011) Resistance exercise enhances mTOR and MAPK signalling in human muscle over that seen at rest after bolus protein ingestion. Acta Physiol (Oxf) 201:365–372

    CAS  Article  Google Scholar 

  120. 120.

    Fusco D, Colloca G, Lo Monaco MR, Cesari M (2007) Effects of antioxidant supplementation on the aging process. Clin Interv Aging 2:377–387

    PubMed  CAS  Google Scholar 

  121. 121.

    Schaap LA, Pluijm SM, Deeg DJ, Visser M (2006) Inflammatory markers and loss of muscle mass (sarcopenia) and strength. Am J Med 119:526.e9–e17

    Google Scholar 

  122. 122.

    Giresi PG, Stevenson EJ, Theilhaber J, Koncarevic A, Parkington J, Fielding RA, Kandarian SC (2005) Identification of a molecular signature of sarcopenia. Physiol Genomics 21:253–263

    PubMed  CAS  Article  Google Scholar 

  123. 123.

    Brink M, Wellen J, Delafontaine P (1996) Angiotensin II causes weight loss and decreases circulating insulin-like growth factor I in rats through a pressor-independent mechanism. J Clin Invest 97:2509–2516

    PubMed  CAS  Article  Google Scholar 

  124. 124.

    Sumukadas D, Witham MD, Struthers AD, McMurdo ME (2007) Effect of perindopril on physical function in elderly people with functional impairment: a randomized controlled trial. CMAJ 177:867–874

    PubMed  Google Scholar 

  125. 125.

    Sumukadas D, Witham MD, Struthers AD, McMurdo ME (2008) Ace inhibitors as a therapy for sarcopenia - evidence and possible mechanisms. J Nutr Health Aging 12:480–485

    PubMed  CAS  Article  Google Scholar 

  126. 126.

    Borst SE (2004) Interventions for sarcopenia and muscle weakness in older people. Age Ageing 33:548–555

    PubMed  Article  Google Scholar 

  127. 127.

    Drummond MJ, Dreyer HC, Pennings B, Fry CS, Dhanani S, Dillon EL, Sheffield-Moore M, Volpi E, Rasmussen BB (2008) Skeletal muscle protein anabolic response to resistance exercise and essential amino acids is delayed with aging. J Appl Physiol 104:1452–1461

    PubMed  CAS  Article  Google Scholar 

  128. 128.

    Gao W, Reiser PJ, Coss CC, Phelps MA, Kearbey JD, Miller DD, Dalton JT (2005) Selective androgen receptor modulator treatment improves muscle strength and body composition and prevents bone loss in orchidectomized rats. Endocrinology 146:4887–4897

    PubMed  CAS  Article  Google Scholar 

  129. 129.

    Langley B, Thomas M, Bishop A, Sharma M, Gilmour S, Kambadur R (2002) Myostatin inhibits myoblast differentiation by down-regulating MyoD expression. J Biol Chem 277:49831–49840

    PubMed  CAS  Article  Google Scholar 

  130. 130.

    Sayer AA, Syddall H, Martin H, Patel H, Baylis D, Cooper C (2008) The developmental origins of sarcopenia. J Nutr Health Aging 12:427–432

    PubMed  CAS  Article  Google Scholar 

Download references

Acknowledgments

The Nutrition Working Group of the IOF Committee of Scientific Advisors was supported by the International Osteoporosis Foundation. The help received from Maria Beloyartseva and Parjeet Kaur in the referencing is gratefully acknowledged.

Conflicts of interest

None.

Author information

Affiliations

  1. Medanta Medicity, Sector 38, Gurgaon, India

    A. Mithal

  2. Division of Bone Diseases, University Hospitals and Faculty of Medicine, Geneva, Switzerland

    J.-P. Bonjour & R. Rizzoli

  3. Centre for Metabolic Bone Diseases and Division of Geriatric Medicine, University of Leuven, Leuven, Belgium

    S. Boonen

  4. Clinique Bois Cerf/Hirslanden, Lausanne, Switzerland

    P. Burckhardt

  5. Institute for Biomedical Research into Human Movement and Health, Manchester Metropolitan University, Manchester, UK

    H. Degens

  6. Division Space Physiology, Institute of Aerospace Medicine, German Aerospace Center, Cologne, Germany

    H. Degens

  7. Calcium Metabolism & Osteoporosis Program, American University of Beirut Medical Center, Beirut, Lebanon

    G. El Hajj Fuleihan

  8. Division of Endocrinology and Metabolism, University of Toronto, St. Michael’s Hospital Health Centre, Toronto, Canada

    R. Josse

  9. Division of Internal Medicine, Endocrine Section, VU University Medical Center, Amsterdam, Netherlands

    P. Lips

  10. Hospital Aranda de la Parra, Hidalgo, León, Mexico

    J. Morales Torres

  11. Department of Joint Disease Research, 22nd Century Medical and Research Center, The University of Tokyo, Tokyo, Japan

    N. Yoshimura

  12. International Osteoporosis Foundation, Nyon, Switzerland

    D. A. Wahl

  13. MRC Lifecourse Epidemiology Unit, University of Southampton, Southampton General Hospital, Southampton, UK

    C. Cooper

  14. NIHR Musculoskeletal Biomedical Research Unit, Institute of Musculoskeletal Sciences, University of Oxford, Oxford, UK

    C. Cooper

  15. Jean Mayer USDA Human Nutrition Research Center on Aging, Tufts University, Boston, MA, USA

    B. Dawson-Hughes

Authors
  1. A. Mithal
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J.-P. Bonjour
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. Boonen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. P. Burckhardt
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. H. Degens
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. G. El Hajj Fuleihan
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. R. Josse
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. P. Lips
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. J. Morales Torres
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. R. Rizzoli
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. N. Yoshimura
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. D. A. Wahl
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. C. Cooper
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. B. Dawson-Hughes
    View author publications

    You can also search for this author in PubMed Google Scholar

Consortia

for the IOF CSA Nutrition Working Group

Corresponding author

Correspondence to A. Mithal.

Additional information

Authors A. Mithal and J.-P. Bonjour contributed equally to the manuscript

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Mithal, A., Bonjour, JP., Boonen, S. et al. Impact of nutrition on muscle mass, strength, and performance in older adults. Osteoporos Int 24, 1555–1566 (2013). https://doi.org/10.1007/s00198-012-2236-y

Download citation

Keywords

  • Aging
  • IOF
  • Malnutrition
  • Muscle strength loss
  • Nutritional
  • Recommendations
  • Sarcopenia