Skip to main content

Advertisement

SpringerLink
Log in

Exercise and nutritional interventions for improving aging muscle health

  • Review
  • Published:
Endocrine Aims and scope Submit manuscript

Abstract

Skeletal muscle mass declines with age (i.e., sarcopenia) resulting in muscle weakness and functional limitations. Sarcopenia has been associated with physiological changes in muscle morphology, protein and hormonal kinetics, insulin resistance, inflammation, and oxidative stress. The purpose of this review is to highlight how exercise and nutritional intervention strategies may benefit aging muscle. It is well known that resistance exercise training increases muscle strength and size and evidence also suggests that resistance training can increase mitochondrial content and decrease oxidative stress in older adults. Recent findings suggest that fast-velocity resistance exercise may be an effective intervention for older adults to enhance muscle power and functional capacity. Aerobic exercise training may also benefit aging skeletal muscle by enhancing mitochondrial bioenergetics, improving insulin sensitivity, and/or decreasing oxidative stress. In addition to exercise, creatine monohydrate, milk-based proteins, and essential fatty acids all have biological effects which could enhance some of the physiological adaptations from exercise training in older adults. Additional research is needed to determine whether skeletal muscle adaptations to increased activity in older adults are further enhanced with effective nutritional interventions and whether this is due to enhanced muscle protein synthesis, improved mitochondrial function, and/or a reduced inflammatory response.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. A.J. Cruz-Jentoft, J.P. Baevens, J.M. Bauer, Y. Boirie, T. Cederholm, F. Landi, F.C. Marin, J.P. Michel, Y. Rolland, S.M. Schneider, E. Topinkova, M. Vandewoude, M. Zamboni, Sarcopenia: European consensus on definitions and diagnosis: report of the European working group on sarcopenia in older people. Age Ageing 39, 412–423 (2010)

    Article  PubMed  Google Scholar 

  2. R.N. Baumgartner, K.M. Koehler, D. Gallagher, L. Romero, S.B. Heymsfield, R.R. Ross, P.J. Gary, R.D. Lindeman, Epidemiology of sarcopenia among the elderly in New Mexico. Am. J. Epidemiol 147, 755–763 (1998)

    Article  PubMed  CAS  Google Scholar 

  3. R.T. Hepple, Sarcopenia—a critical perspective. Sci. Aging Knowl. Environ. 19, 31 (2003)

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  5. L.J. Melton 3rd, S. Khosla, C.S. Crowson, M.K. O’Connor, W.M. O’Fallon, B.L. Riggs, Epidemiology of sarcopenia. J. Am. Geriatr. Soc. 48, 625–630 (2000)

    PubMed  Google Scholar 

  6. E.M. Lau, H.S. Lynn, J.W. Woo, T.C. Kwok, L.J. Melton 3rd, Prevalence of and risk factors for sarcopenia in elderly Chinese men and women. J. Gerontol. A Biol. Sci. Med. Sci. 60, 213–216 (2005)

    Article  PubMed  Google Scholar 

  7. M.A. Tarnopolsky, A. Safdar, The potential benefits of creatine and conjugated linoleic acid as adjuncts to resistance training in older adults. Appl. Physiol. Nutr. Metab. 33, 213–227 (2008)

    Article  PubMed  CAS  Google Scholar 

  8. I. Janssen, D.S. Shepard, P.T. Katzmarzyk, R. Roubenoff, The healthcare costs of sarcopenia in the United States. J. Am. Geriatr. Soc. 52, 80–85 (2004)

    Article  PubMed  Google Scholar 

  9. C.W. Bales, C.S. Ritchie, Sarcopenia, weight loss, and nutritional frailty in the elderly. Ann. Rev. Nutr. 22, 309–323 (2002)

    Article  CAS  Google Scholar 

  10. P.G. Giresi, E.J. Stevenson, J. Theilhaber, A. Koncarevic, J. Parkington, R.A. Fiedling, S.C. Kandarian, Identification of a molecular signature of sarcopenia. Physiol. Genomics 1421, 253–263 (2005)

    Google Scholar 

  11. J. Aiken, E. Bua, Z. Cao, M. Lopez, J. Wanagat, D. McKenzie, S. Mckiernan, Mitochondrial DNA deletion mutations and sarcopenia. Ann. NY. Acad. Sci. 959, 412–423 (2002)

    Article  PubMed  CAS  Google Scholar 

  12. K. Ohlendieck, Proteomics of skeletal muscle differentiation, neuromuscular disorders and fiber aging. Expert. Rev. Proteomics 7, 283–296 (2010)

    Article  PubMed  CAS  Google Scholar 

  13. P. Balagopal, D. Proctor, K.S. Nair, Sarcopenia and hormonal changes. Endocrine 7, 57–60 (1997)

    Article  PubMed  CAS  Google Scholar 

  14. E. Ziv, D. Hu, Genetic variation in insulin/IGF-1 signaling pathways and longevity. Ageing. Res. Rev. 10, 201–204 (2011)

    Article  PubMed  CAS  Google Scholar 

  15. A.M. Abbatecola, G. Paolisso, P. Fattoretti, W.J. Evans, V. Fiore, L. Dicioccio, F. Lattanzio, Discovering pathways of sarcopenia in older adults: a role for insulin resistance on mitochondria dysfunction. J. Nutr. Health Aging 15, 890–895 (2011)

    Article  PubMed  CAS  Google Scholar 

  16. L.J. Greenlund, K.S. Nair, Sarcopenia—consequences, mechanisms, and potential therapies. Mech. Ageing Dev. 124, 287–299 (2003)

    Article  PubMed  CAS  Google Scholar 

  17. C. Gelfi, A. Vigano, M. Ripamonti, A. Pontoglio, S. Begum, M.A. Pellegrino, B. Grassi, R. Bottinelli, R. Wait, P. Cerretelli, The human muscle proteome in aging. J. Proteome Res. 5, 1344–1353 (2006)

    Article  PubMed  CAS  Google Scholar 

  18. D.G. Candow, J.P. Little, P.D. Chilibeck, S. Abeysekara, G.A. Zello, S. Kazachkov, S.M. Cornish, P.H. Yu, Low-dose creatine combined with protein during resistance training in older men. Med. Sci. Sports Exerc. 40, 1645–1652 (2008)

    Article  PubMed  CAS  Google Scholar 

  19. D.G. Candow, P.D. Chilibeck, M. Facci, S. Abeysekara, G.A. Zello, Protein supplementation before and after resistance training in older men. Eur. J. Appl. Physiol. 97, 548–556 (2006)

    Article  PubMed  CAS  Google Scholar 

  20. W.R. Frontera, C.N. Meredith, K.P. O’Reilly, H.G. Knuttgen, W.J. Evans, Strength conditioning in older men: skeletal muscle hypertrophy and improved function. J. Appl. Physiol. 64, 1038–1044 (1988)

    PubMed  CAS  Google Scholar 

  21. M.A. Fiatarone, E.F. O’Neill, N.D. Ryan, K.M. Clements, G.R. Solares, M.E. Nelson, S.B. Roberts, J.J. Kehayias, L.A. Lipsitz, W.J. Evans, Exercise training and nutritional supplementation for physical frailty in very elderly people. N. Engl. J. Med. 330, 1769–1775 (1994)

    Article  PubMed  CAS  Google Scholar 

  22. S.L. Charette, L. McEvoy, G. Pyka, C. Snow-Harter, D. Guido, R.A. Wiswell, R. Marcus, Muscle hypertrophy response to resistance training in older women. J. Appl. Physiol. 70, 1912–1916 (1991)

    PubMed  CAS  Google Scholar 

  23. W.J. Evans, What is sarcopenia? J. Gerontol. A Biol. Sci. Med. Sci. 50, 5–8 (1995)

    Article  PubMed  Google Scholar 

  24. W.W. Campbell, L.J. Joseph, S.L. Davey, D. Cyr-Campbell, R.A. Anderson, W.J. Evans, Effects of resistance training and chromium picolinate on body composition and skeletal muscle in older men. J. Appl. Physiol. 86, 29–39 (1999)

    PubMed  CAS  Google Scholar 

  25. K.E. Yarasheski, J. Pak-Loduca, D.L. Hasten, K.A. Obert, M.B. Brown, D.R. Sinacore, Resistance exercise training increases mixed muscle protein synthesis rate in frail women and men >/=76 yr old. Am. J. Physiol. 277, E118–E125 (1999)

    PubMed  CAS  Google Scholar 

  26. J.N. Schulte, K.E. Yarasheski, Effects of resistance training on the rate of muscle protein synthesis in frail elderly people. Int J Sport Nutr Exerc. Metab. 11, S111–S118 (2001)

    PubMed  Google Scholar 

  27. L.B. Verdijk, B.G. Gleeson, R.A. Jonkers, K. Meijer, H.H. Savelberg, P. Dendale, L.J. van Loon, Skeletal muscle hypertrophy following resistance training is accompanied by a fibre type-specific increase in satellite cell content in elderly men. J. Gerontol. A Biol. Sci. Med. Sci. 64, 332–339 (2009)

    Article  PubMed  CAS  Google Scholar 

  28. I. Smilios, T. Pilianidis, M. Karamouzis, A. Parlavantzas, S.P. Tokmakidis, Hormonal responses after a strength endurance resistance exercise protocol in young and elderly males. Int. J. Sports Med. 28, 401–406 (2007)

    Article  PubMed  CAS  Google Scholar 

  29. S.M. Cornish, P.D. Chilibeck, Alpha-linolenic acid supplementation and resistance training in older adults. Appl. Physiol. Nutr. Metab. 34, 49–59 (2009)

    Article  PubMed  CAS  Google Scholar 

  30. A. Brose, G. Parise, M.A. Tarnopolsky, Creatine supplementation enhances isometric strength and body composition improvements following strength exercise training in older adults. J. Gerontol. A Biol. Sci. Med. Sci. 58, 11–19 (2003)

    Article  PubMed  Google Scholar 

  31. M. Tarnopolsky, A. Zimmer, J. Paikin, A. Safdar, A. Aboud, E. Pearce, B. Roy, T. Doherty, Creatine monohydrate and conjugated linoleic acid improve strength and body composition following resistance exercise in older adults. PLoS ONE 2, 991 (2007)

    Article  CAS  Google Scholar 

  32. N. McCartney, A.L. Hicks, J. Martin, C.E. Webber, A longitudinal trial of weight training in the elderly: continued improvements in year 2. J. Gerontol. A Biol. Sci. Med. Sci. 51, B425–B433 (1996)

    Article  PubMed  CAS  Google Scholar 

  33. D.G. Candow, P.D. Chilibeck, S. Abeysekara, G.A. Zello, Short-term heavy resistance training eliminates age-related deficits in muscle mass and strength in healthy older males. J. Strength Cond. Res. 25, 326–333 (2011)

    Article  PubMed  Google Scholar 

  34. S.P. Sayers, High-speed power training: a novel approach to resistance training in older men and women. A brief review and pilot study. J. Strength Cond. Res. 21, 518–526 (2007)

    PubMed  Google Scholar 

  35. M.M. Porter, Power training for older adults. Appl. Physiol. Nutr. Metab. 31, 87–94 (2006)

    Article  PubMed  Google Scholar 

  36. E.J. Metter, R. Conwit, J. Tobin, J.L. Fozard, Age-associated loss of power and strength in the upper extremities in women and men. J. Gerontol. A Biol. Sci. Med. Sci. 52, B267–B276 (1997)

    Article  PubMed  CAS  Google Scholar 

  37. A.P. Johnston, M. De Lisio, G. Parise, Resistance training, sarcopenia, and the mitochondrial theory of aging. Appl. Physiol. Nutr. Metab. 33, 191–199 (2008)

    Article  PubMed  CAS  Google Scholar 

  38. L. Staunton, K. O’Connell, K. Ohlendieck, Proteomic profiling of mitochondrial enzymes during skeletal muscle aging. J. Aging. Res. (2011). doi:10.4061/2011/908035

    PubMed  Google Scholar 

  39. J.O. Holloszy, Biochemical adaptations in muscle. Effects of exercise on mitochondrial oxygen uptake and respiratory enzyme activity in skeletal muscle. J. Biol. Chem. 242, 2278–2282 (1967)

    PubMed  CAS  Google Scholar 

  40. J.O. Holloszy, F.W. Booth, Biochemical adaptations to endurance exercise in muscle. Annu. Rev. Physiol. 38, 273–291 (1976)

    Article  PubMed  CAS  Google Scholar 

  41. K.R. Short, J.L. Vittone, M.L. Bigelow, D.N. Proctor, R.A. Rizza, J.M. Coenen-Schimke, K.S. Nair, Impact of aerobic exercise training on age-related changes in insulin sensitivity and muscle oxidative capacity. Diabetes 52, 1888–1896 (2003)

    Article  PubMed  CAS  Google Scholar 

  42. I.R. Lanza, D.K. Short, K.R. Short, S. Raghavakaimal, R. Basu, M.J. Joyner, J.P. McConnell, K.S. Nair, Endurance exercise as a countermeasure for aging. Diabetes 57, 2933–2942 (2008)

    Article  PubMed  CAS  Google Scholar 

  43. D.A. Hood, I. Irrcher, V. Ljubicic, A.M. Joseph, Coordination of metabolic plasticity in skeletal muscle. J. Exp. Biol. 209, 2265–2275 (2006)

    Article  PubMed  CAS  Google Scholar 

  44. J.A. Hawley, M. Hargreaves, J.R. Zierath, Signalling mechanisms in skeletal muscle: role in substrate selection and muscle adaptation. Essays Biochem. 42, 1–12 (2006)

    Article  PubMed  CAS  Google Scholar 

  45. V.A. Lira, C.R. Benton, Z. Yan, A. Bonen, PGC-1alpha regulation by exercise training and its influences on muscle function and insulin sensitivity. Am. J. Physiol. Endocrinol. Metab. 299, E145–E161 (2010)

    PubMed  CAS  Google Scholar 

  46. J.P. Little, A. Safdar, N. Cermak, M.A. Tarnopolsky, M.J. Gibala, Acute endurance exercise increases the nuclear abundance of PGC-1aplpha in trained human skeletal muscle. Am. J. Physiol. Regul. Integr. Comp. Physiol. 298, R912–R917 (2010)

    Article  PubMed  CAS  Google Scholar 

  47. H. Pilegaard, B. Saltin, P.D. Neufer, Exercise induces transient transcriptioin activation of PGC-1alpha gene in human skeletal muscle. J. Physiol. 546, 851–858 (2003)

    Article  PubMed  CAS  Google Scholar 

  48. D.J. Baker, A.C. Betik, D.J. Krause, R.T. Hepple, No decline in skeletal muscle oxidative capacity with aging in long-term calorically restricted rats: effects are independent of mitochondrial DNA integrity. J. Gerontol. A. Biol. Med.Sci. 61, 657–684 (2006)

    Google Scholar 

  49. K.S. Nair, Aging muscle. Am. J. Clin. Nutr. 81, 953–963 (2005)

    PubMed  CAS  Google Scholar 

  50. C. Leeuwenburgh, J.W. Heinecke, Oxidative stress and antioxidants in exercise. Curr. Med. Chem. 8, 829–838 (2001)

    PubMed  CAS  Google Scholar 

  51. A. Safdar, M.J. Hamadeh, J.J. Kaczor, S. Raha, J. deBeer, M.A. Tarnopolsky, Aberrant mitochondrial homeostasis in the skeletal muscle of sedentary older adults. PLoS ONE 5, e10778 (2010)

    Article  PubMed  CAS  Google Scholar 

  52. A. Abadi, E.I. Glover, R.J. Isfort, S. Raha, A. Safdar, N. Yasuda, J.J. Kaczor, S. Melov, A. Hubbard, X. Qu, S.M. Phillips, M. Tarnopolsky, Limb immobilization induces a coordinate down-regulation of mitochondrial and other metabolic pathways in men and women. PLoS ONE 4, e6518 (2009)

    Article  PubMed  CAS  Google Scholar 

  53. T. Wenz, S.G. Rossi, R.L. Rotundo, B.M. Spiegelman, C.T. Moraes, Increased muscle PGC-1alpha expression protects from sarcopenia and metabolic disease during aging. Proc. Natl. Acad. Sci. USA 106, 20405–20410 (2009)

    Article  PubMed  CAS  Google Scholar 

  54. M. Sandri, J. Lin, C. Handschin, W. Yang, Z.P. Arany, S.H. Lecker, A.L. Goldberg, B.M. Spiegelman, PGC-1alpha protects skeletal muscle from atrophy by suppressing FoxO3 action and atrophy-specific gene transcription. Proc. Natl. Acad. Sci. USA 103, 16260–16265 (2006)

    Article  PubMed  CAS  Google Scholar 

  55. J.A. Hawley, Exercise as a therapeutic intervention for the prevention and treatment of insulin resistance. Diabetes. Metab. Res. Rev. 20, 383–393 (2004)

    Article  PubMed  CAS  Google Scholar 

  56. J.O. Holloszy, Exercise-induced increase in muscle insulin sensitivity. J. Appl. Physiol. 99, 338–343 (2005)

    Article  PubMed  CAS  Google Scholar 

  57. B. Hildrum, A. Mykletun, T. Hole, K. Midthjell, A.A. Dahl, Age-specific prevalence of the metabolic syndrome defined by the International Diabetes Federation and the National Cholesterol Education Program: the Norwegian HUNT 2 study. B.M.C. Public Health 7, 220 (2007)

    Article  Google Scholar 

  58. P.L. Greenhaff, L.G. Karagounis, N. Peirce, E.J. Simpson, M. Hazell, R. Layfield, H. Wackerhage, K. Smith, P. Atherton, A. Selby, M.J. Rennie, Disassociation between the effects of amino acids and insulin on signaling, ubiquitin ligases, and protein turnover in human muscle. Am. J. Physiol. Endocrinol. Metab. 295, E595–E604 (2008)

    Article  PubMed  CAS  Google Scholar 

  59. W.M. Bennet, A.A. Connacher, C.M. Scrimgeour, R.T. Jung, M.J. Rennie, Euglycemic hyperinsulinemia augments amino acid uptake by human leg tissues during hyperaminoacidemia. Am. J. Physiol. 259, E185–E194 (1990)

    PubMed  CAS  Google Scholar 

  60. G. Biolo, Declan Fleming, R.Y., Wolfe, R.R.: Physiologic hyperinsulinemia stimulates protein synthesis and enhances transport of selected amino acids in human skeletal muscle. J. Clin. Invest. 95, 811–819 (1995)

    Article  PubMed  CAS  Google Scholar 

  61. K.A. Burgomaster, K.R. Howarth, S.M. Phillips, M. Rakobowchuk, M.J. Macdonald, S.L. McGee, M.J. Gibala, Similar metabolic adaptations during exercise after low volume sprint interval and traditional endurance training in humans. J. Physiol. 586, 151–160 (2008)

    Article  PubMed  CAS  Google Scholar 

  62. J.P. Little, A. Safdar, G.P. Wilkin, M.A. Tarnopolsky, M.J. Gibala, A practical model of low-volume high-intensity interval training induces mitochondrial biogenesis in human skeletal muscle: potential mechanisms. J. Physiol. 588, 1011–1022 (2010)

    Article  PubMed  CAS  Google Scholar 

  63. J.P. Little, A.J. Cochran, Regulating the regulators: the role of transcriptional regulatory proteins in the adaptive response to exercise in human skeletal muscle. J. Physiol. 589, 1511–1512 (2011)

    Article  PubMed  CAS  Google Scholar 

  64. J.P. Little, A. Safdar, D. Bishop, M.A. Tarnopolsky, M.J. Gibala, An acute bout of high-intensity interval training increases the nuclear abundance of PGC-1alpha and activates mitochondrial biogenesis in human skeletal muscle. Am. J. Physiol. Regul. Integr. Comp. Physiol. 300, R1303–R1310 (2011)

    Article  PubMed  CAS  Google Scholar 

  65. J.P. Little, J.B. Gillen, M.E. Percival, A. Safdar, M.A. Tarnopolsky, Z. Punthakee, M.E. Jung, M.J. Gibala, Low-volume high-intensity interval training reduces hyperglycemia and increases muscle mitochondrial capacity in patients with type 2 diabetes. J. Appl. Physiol. 111, 1554–1560 (2011)

    Article  PubMed  CAS  Google Scholar 

  66. M.S. Hood, J.P. Little, M.A. Tarnopolsky, F. Myslik, M.J. Gibala, Low-volume interval training improves muscle oxidative capacity in sedentary adults. Med. Sci. Sports Exerc. 43, 1849–1856 (2011)

    Article  PubMed  CAS  Google Scholar 

  67. J.C. Richards, T.K. Johnson, J.N. Kuzma, M.C. Lonac, M.M. Schweder, W.F. Voyles, C. Bell, Short-term sprint interval training increases insulin sensitivity in healthy adults but does not affect the thermogenic response to beta-adrenergic stimulation. J. Physiol. 588, 2961–2972 (2010)

    Article  PubMed  CAS  Google Scholar 

  68. M. Wyss, R. Kaddurah-Daouk, Creatine and creatinine metabolism. Physiol. Rev. 80, 1107–1213 (2000)

    PubMed  CAS  Google Scholar 

  69. S.A. Smith, S.J. Montain, R.P. Matott, G.P. Zientara, F.A. Jolesz, R.A. Fielding, Creatine supplementation and age influence muscle metabolism during exercise. J. Appl. Physiol. 85, 1349–1356 (1998)

    PubMed  CAS  Google Scholar 

  70. J.L. Vierck, D.L. Icenoggle, L. Bucci, M.V. Dodson, The effects of ergogenic compounds on myogenic satellite cells. Med. Sci. Sports Exerc. 34, 769–776 (2003)

    Article  CAS  Google Scholar 

  71. B. Dangott, E. Schultz, P.E. Mozdziak, Dietary creatine monohydrate supplementation increases satellite cell mitotic activity during compensatory hypertrophy. Int. J. Sports Med. 21, 13–16 (2000)

    Article  PubMed  CAS  Google Scholar 

  72. S. Olsen, P. Aagaard, F. Kadi, G. Tufekovic, J. Verney, J.L. Olesen, C. Suetta, M. Kjaer, Creatine supplementation augments the increase in satellite cell and myonuclei number in human skeletal muscle induced by strength training. J. Physiol. 573, 525–534 (2006)

    Article  PubMed  CAS  Google Scholar 

  73. D.S. Willoughby, J.M. Rosene, Effect of oral creatine and resistance training on myogenic regulatory factor expression. Med. Sci. Sports Exerc. 35, 923–929 (2003)

    Article  PubMed  CAS  Google Scholar 

  74. D.G. Burke, D.G. Candow, P.D. Chilibeck, L.G. MacNeil, B.D. Roy, M.A. Tarnopolsky, T. Ziegenfuss, Effect of creatine supplementation and resistance-exercise training on muscle insulin-like growth factor in young adults. Int J Sport Nutr Exerc. Metab. 18, 389–398 (2008)

    Article  PubMed  CAS  Google Scholar 

  75. G. Parise, S. Mihic, D. MacLennan, K.E. Yarasheski, M.A. Tarnopolsky, Effects of acute creatine monohydrate supplementation on leucine kinetics and mixed-muscle protein synthesis. J. Appl. Physiol. 91, 1041–1047 (2001)

    PubMed  CAS  Google Scholar 

  76. R.A. Bassit, R. Curi, L.F. Costa Rosa, Creatine supplementation reduces plasma levels of pro-inflammatory cytokines and PGE2 after a half-ironman competition. Amino Acids 35, 425–431 (2008)

    Article  PubMed  CAS  Google Scholar 

  77. R.V. Santos, R.A. Bassit, E.C. Caperuto, L.F. Costa Rosa, The effect of creatine supplementation upon inflammatory and muscle soreness markers after a 30 km race. Life Sci. 75, 1917–1924 (2004)

    Article  PubMed  CAS  Google Scholar 

  78. S. Sipila, M. Elorinne, M. Alen, H. Suominen, V. Kovanen, Effects of strength and endurance training on muscle fibre characteristics in elderly women. Clin. Physiol. 17, 459–474 (1997)

    Article  PubMed  CAS  Google Scholar 

  79. D.G. Candow, P.D. Chilibeck, Review: timing of creatine and protein supplementation during resistance training in the elderly. Appl. Physiol. Nutr. Metab. 33, 184–190 (2008)

    Article  PubMed  CAS  Google Scholar 

  80. M.J. Church, P.D. Chilibeck, K.E. Chad, K.S. Davison, D.G. Burke, Creatine supplementation combined with resistance training in older men. Med. Sci. Sports Exerc. 33, 2111–2117 (2001)

    Article  Google Scholar 

  81. P. Hespel, B.O. Eijnde, W. Derave, E.A. Richter, Creatine supplementation: exploring the role of the creatine kinase/phosphocreatine system in human muscle. Can. J. Appl. Physiol. 26 suppl, S79–102 (2001)

    PubMed  CAS  Google Scholar 

  82. A. Mauro, Satellite cell of skeletal muscle fibers. J. Biophys. Biochem. Cytol. 9, 493–495 (1961)

    Article  PubMed  CAS  Google Scholar 

  83. J.G. Ryall, J.D. Schertzer, G.S. Lynch, Cellular and molecular mechanisms underlying age-related skeletal muscle wasting and weakness. Biogerontology 9, 213–228 (2008)

    Article  PubMed  CAS  Google Scholar 

  84. A.S. Brack, T.A. Rando, Intrinsic changes and extrinsic influences of myogenic stem cell function during aging. Stem Cell Rev. 3, 226–237 (2007)

    Article  PubMed  CAS  Google Scholar 

  85. G.E. Butterfield, J. Thompson, M.J. Rennie, R. Marcus, R.L. Hintz, A.R. Hoffman, Effect of rhGH and rhIGF-1 treatment on protein utilization in elderly women. Am. J. Physiol. 272, E94–E99 (1997)

    PubMed  CAS  Google Scholar 

  86. C.A. Greig, P.J. Atherton, M.J. Rennie, Can an NSAID a day keep muscle wasting away? J. Physiol. 587, 5483–5492 (2009)

    Article  CAS  Google Scholar 

  87. I. Bautmans, R. Njemini, S. Vasseur, H. Chabert, L. Moens, C. Demanet, T. Mets, Biochemical changes in response to intensive resistance exercise training in the elderly. Gerontology 51, 253–265 (2005)

    Article  PubMed  CAS  Google Scholar 

  88. K.J. Ladner, M.A. Califiuri, D.C. Guttridge, Tumor necrosis factor-regulated biphasic activation of NF-kappa B is required for cytokine-induced loss of skeletal muscle gene products. J. Biol. Chem. 278, 2294–2303 (2003)

    Article  PubMed  CAS  Google Scholar 

  89. R. Rahimi, Creatine supplementation decreases oxidative DNA damage and lipid peroxidation induced by a single bout of resistance exercise. J. Strength Cond. Res. 25, 3448–3455 (2011)

    Article  PubMed  Google Scholar 

  90. C. Kang, K.M. O’Moore, J.R. Dickman, L.L. Ji, Exercise activation of muscle peroxisome proliferator-activated receptor-gamma coactivator-1alpha signaling is redox sensitive. Free Radic. Biol. Med. 47, 1394–1400 (2009)

    Article  PubMed  CAS  Google Scholar 

  91. R. Deminice, A. A. Jordao, Creatine supplementation reduces oxidative stress biomarkers after acute exercise in rats. Amino Acids (2011). [Epub ahead of print]

  92. P. Sestili, C. Martinelli, E. Colombo, E. Barbieri, L. Potenza, S. Sartini, C. Fimognari, Creatine as an antioxidant. Amino Acids 40, 1385–1396 (2011)

    Article  PubMed  CAS  Google Scholar 

  93. C. Fimognari, P. Sestili, M. Lenzi, G. Cantelli-Forti, P. Hrelia, Protective effect of creatine against RNA damage. Mutat. Res. 670, 59–67 (2009)

    Article  PubMed  CAS  Google Scholar 

  94. L. Vergnani, S. Hatrik, F. Ricci, A. Passaro, N. Manzoli, G. Zuliani, V. Brovkovych, R. Fellin, T. Malinski, Effect of native and oxidized low-density lipoprotein on endothelial nitric oxide and superoxide production: key role of l-arginine availability. Circulation 101, 1261–1266 (2000)

    Article  PubMed  CAS  Google Scholar 

  95. American College of Rheumatology, Recommendation for the medical management of osteoarthritis of the hip and knee: 2000 update. American College of Rheumatology Subcommittee on Osteoarthritis Guidelines. Arthritis. Rheum. 43, 1905–1915 (2000)

    Article  Google Scholar 

  96. N. Arden, M.C. Nevitt, Osteoarthritis: epidemiology. Best Pract. Res. Clin. Rheumatol. 20, 3–25 (2006)

    Article  PubMed  Google Scholar 

  97. B. Willer, G. Stucki, H. Hoppeler, P. Bruhlmann, S. Krahenbuhl, Effects of creatine supplementation on muscle weakness in patients with rheumatoid arthritis. Rheumatology (Oxford) 39, 293–298 (2000)

    Article  CAS  Google Scholar 

  98. M. Neves Jr, B. Gualano, H. Roschel, R. Fuller, F.B. Benatti, A.L. de Sa Pinto, F.R. Lima, R.M. Pereira, A.H. Lancha Jr, E. Bonfa, Beneficial effect of creatine supplementation in knee osteoarthritis. Med. Sci. Sports Exerc. 43, 1538–1543 (2011)

    Article  PubMed  CAS  Google Scholar 

  99. D.J. Millward, Sufficient protein for our elders? Am. J. Clin. Nutr. 88, 1187–1188 (2008)

    PubMed  CAS  Google Scholar 

  100. E. Borsheim, K.D. Tipton, S.E. Wolf, R.R. Wolfe, Essential amino acids and muscle protein recovery from resistance exercise. Am. J. Physiol. 283, E648–E657 (2002)

    CAS  Google Scholar 

  101. E. Volpi, H. Kobayashi, M. Sheffield-Moore, B. Mittendorfer, R.R. Wolfe, Essential amino acids are primarily responsible for the amino acid stimulation of muscle protein anabolism in healthy elderly adults. Am. J. Clin. Nutr. 78, 250–258 (2003)

    PubMed  CAS  Google Scholar 

  102. S. Fujita, H.C. Dreyer, M.J. Drummond, E.L. Glynn, J.G. Cadenas, F. Yoshizawa, E. Volpi, B.B. Rasmussen, Nutrient signalling in the regulation of human muscle protein synthesis. J. Physiol. 582, 813–823 (2007)

    Article  PubMed  CAS  Google Scholar 

  103. P. Gran, D. Cameron-Smith, The actions of exogenous leucine on mTOR signalling and amino acid transporters in human myotubes. B.M.C. Physiol. 11, 10 (2011)

    CAS  Google Scholar 

  104. H.C. Dreyer, M.J. Drummond, B. Pennings, S. Fujita, E.L. Glynn, D.L. Chinkes, S. Dhanani, E. Volpi, B.B. Rasmussen, Leucine-enriched essential amino acid and carbohydrate ingestion following resistance exercise enhances mTOR signaling and protein synthesis in human muscle. Am. J. Physiol. 294, E392–E400 (2008)

    CAS  Google Scholar 

  105. S.M. Phillips, J.E. Tang, D.R. Moore, The role of milk- and soy-based protein in support of muscle protein synthesis and muscle protein accretion in young and elderly persons. J. Am. Coll. Nutr. 28, 343–354 (2009)

    PubMed  CAS  Google Scholar 

  106. C.S. Katsanos, H. Kobayashi, M. Sheffield-Moore, A. Aarsland, R.R. Wolfe, 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. 291, E381–E387 (2006)

    CAS  Google Scholar 

  107. J.P. Little, S.M. Phillips, Resistance exercise and nutrition to counteract muscle wasting. Appl. Physiol. Nutr. Metab. 34, 817–828 (2009)

    Article  PubMed  Google Scholar 

  108. S.M. Phillips, J.W. Hartman, S.B. Wilkinson, Dietary protein to support anabolism with resistance exercise in young men. J. Am. Coll. Nutr. 24, 134S–139S (2005)

    PubMed  Google Scholar 

  109. J.E. Tang, D.R. Moore, G.W. Kujbida, M.A. Tarnopolsky, S.M. Phillips, Ingestion of whey hydrolysate, casein, or soy protein isolate: effects on mixed muscle protein synthesis at rest and following resistance exercise in young men. J. Appl. Physiol. 107, 987–992 (2009)

    Article  PubMed  CAS  Google Scholar 

  110. D.W. West, N.A. Burd, V.G. Coffey, S.K. Baker, L.M. Burke, J.A. Hawley, D.R. Moore, T. Stellingwerff, S.M. Phillips, Rapid aminoacidemia enhances myofibrillar protein synthesis and anabolic intramuscular signaling responses after resistance exercise. Am. J. Clin. Nutr. 94, 795–803 (2011)

    Article  PubMed  CAS  Google Scholar 

  111. J.W. Hartman, J.E. Tang, S.B. Wilkinson, M.A. Tarnopolsky, R.L. Lawrence, A.V. Fullerton, S.M. Phillips, Consumption of fat-free fluid milk after resistance exercise promotes greater lean mass accretion than does consumption of soy or carbohydrate in young, novice, male weight lifters. Am. J. Clin. Nutr. 86, 373–381 (2007)

    PubMed  CAS  Google Scholar 

  112. S. Kukuljan, C.A. Nowson, K. Sanders, R.M. Daly, Effects of resistance exercise and fortified milk on skeletal muscle mass, muscle size, and functional performance in middle-aged and older men: an 18-mo randomized controlled trial. J. Appl. Physiol. 107, 1864–1873 (2009)

    Article  PubMed  CAS  Google Scholar 

  113. K.D. Tipton, B.B. Rasmussen, S.L. Miller, S.E. Wolf, S.K. Owens-Stovall, B.E. Petrini, R.R. Wolfe, Timing of amino acid-carbohydrate ingestion alters anabolic response of muscle to resistance exercise. Am. J. Physiol. Endocrinol. Metab. 281, E197–E206 (2001)

    PubMed  CAS  Google Scholar 

  114. M.J. Rennie, H. Wackerhage, E.E. Spangenburg, F.W. Booth, Control of the size of the human muscle mass. Annu. Rev. Physiol. 66, 799–828 (2004)

    Article  PubMed  CAS  Google Scholar 

  115. Y. Yang, L. Breen, N.A. Burd, A.J. Hector, T.A. Churchward-Venne, A.R. Josse, M.A. Tarnopolsky, S.M. Phillips, Resistance exercise enhances myofibrillar protein synthesis with graded intakes of whey protein in older men. Br. J. Nutr. 7, 1–9 (2012)

    Article  Google Scholar 

  116. D.R. Moore, M.J. Robinson, J.L. Fry, J.E. Tang, E.I. Glover, S.B. Wilkinson, T. Prior, M.A. Tarnopolsky, S.M. Phillips, Ingested protein dose response of muscle and albumin protein synthesis after resistance exercise in young men. Am. J. Clin. Nutr. 89, 161–168 (2009)

    Article  PubMed  CAS  Google Scholar 

  117. R.C. Bunn, G.E. Cockrell, Y. Ou, K.M. Thrailkill, C.K. Lumpkin Jr, J.L. Fowlkes, Palmitate and insulin synergistically induce IL-6 expression in human monocytes. Cardiovasc. Diabetol. 9, 73 (2010)

    Article  PubMed  CAS  Google Scholar 

  118. L. Haversen, K.N. Danielsson, L. Fogelstrand, O. Wiklund, Induction of proinflammatory cytokines by long-chain saturated fatty acids in human macrophages. Atherosclerosis 202, 382–393 (2009)

    Article  PubMed  CAS  Google Scholar 

  119. T. Coll, E. Eyre, R. Rodriguez-Calvo, X. Palomer, R.M. Sanchez, M. Merlos, J.C. Laguna, M. Vazguez-Carrera, Oleate reverses palmitate-induced insulin resistance and inflammation in skeletal muscle cells. J. Biol. Chem. 283, 11107–11116 (2008)

    Article  PubMed  CAS  Google Scholar 

  120. T. Phillips, C. Leeuwenburgh, Muscle fiber-specific apoptosis and TNF-alpha signaling in sarcopenia are attenuated by life-long calorie restriction. FASEB J. 19, 668–670 (2005)

    PubMed  CAS  Google Scholar 

  121. L. Deldicque, P.D. Cani, A. Philp, J.M. Raymackers, P.J. Meakin, M.L. Ashford, N.M. Delzenne, M. Francaux, K. Baar, The unfolded protein response is activated in skeletal muscle by high-fat feeding: potential role in the downregulation of protein synthesis. Am. J. Physiol. Endocrinol. Metab. 299, E695–E705 (2010)

    Article  PubMed  CAS  Google Scholar 

  122. M. Sitnick, S.C. Bodine, J.C. Rutledge, Chronic high fat feeding attenuates load-induced hypertrophy in mice. J. Physiol. 587, 5753–5765 (2009)

    Article  PubMed  CAS  Google Scholar 

  123. C.S. Fry, M.J. Drummond, E.L. Glynn, J.M. Dickinson, D.M. Gundermann, K.L. Timmerman, D.K. Walker, S. Dhanani, E. Volpi, B.B. Rasmussen, Aging impairs contraction-induced human skeletal muscle mTORC1 signalling and protein synthesis. Skelet. Muscle 1, 11 (2011)

    Article  PubMed  CAS  Google Scholar 

  124. G.I. Smith, P. Atherton, D.N. Reeds, B.S. Mohammed, D. Rankin, M.J. Rennie, B. Mittendorfer, Dietary omega-3 fatty acid supplementation increases the rate of muscle protein synthesis in older adults: a randomized controlled trial. Am. J. Clin. Nutr. 93, 402–412 (2011)

    Article  PubMed  CAS  Google Scholar 

  125. N. Tardif, J. Salles, J.F. Landrier, I. Mothe-Satney, C. Guillet, C. Boue-Vaysse, L. Combaret, C. Giraudet, V. Patrac, J. Bertrand-Michel, C. Migne, J.M. Chardigny, Y. Boirie, S. Walrand, Oleate-enriched diet improves insulin sensitivity and restores muscle protein synthesis in old rats. Clin. Nutr. 30, 799–806 (2011)

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Faculty of Physical Education and Recreation, University of Alberta, Edmonton, Canada

    Scott C. Forbes

  2. Irving K. Barber School of Arts and Sciences, University of British Columbia-Okanagan, Kelowna, Canada

    Jonathan P. Little

  3. Faculty of Kinesiology and Health Studies, Centre on Aging and Health, University of Regina, Regina, SK, S4S 0A2, Canada

    Darren G. Candow

Authors
  1. Scott C. Forbes
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jonathan P. Little
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Darren G. Candow
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Darren G. Candow.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Forbes, S.C., Little, J.P. & Candow, D.G. Exercise and nutritional interventions for improving aging muscle health. Endocrine 42, 29–38 (2012). https://doi.org/10.1007/s12020-012-9676-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12020-012-9676-1

Keywords

Search

Navigation