Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-26T07:00:02.511Z Has data issue: false hasContentIssue false
  • English
  • Français

The developmental origins of sarcopenia: from epidemiological evidence to underlying mechanisms

Published online by Cambridge University Press:  05 March 2010

A. A. Sayer ,
C. Stewart ,
H. Patel  and
C. Cooper
A. A. Sayer*
Affiliation:
Ageing and Health, MRC Epidemiology Resource Centre, MRC Epidemiology Resource Centre, University of Southampton, Southampton, UK
C. Stewart
Affiliation:
Molecular and Cell Biology, Institute for Biomedical Research into Human Movement and Health, Manchester Metropolitan University, Manchester, UK
H. Patel
Affiliation:
Ageing and Health, MRC Epidemiology Resource Centre, MRC Epidemiology Resource Centre, University of Southampton, Southampton, UK
C. Cooper
Affiliation:
Ageing and Health, MRC Epidemiology Resource Centre, MRC Epidemiology Resource Centre, University of Southampton, Southampton, UK
*
Address for correspondence: A. A. Sayer, MRC Epidemiology Resource Centre, University of Southampton, Southampton, SO16 6YD, UK. (Email [email protected])
Get access Rights & Permissions [Opens in a new window]

Abstract

Sarcopenia is defined as the loss of skeletal muscle mass and strength with age. There is increasing recognition of the serious health consequences in terms of disability, morbidity and mortality as well as major healthcare costs. Adult determinants of sarcopenia including age, gender, size, levels of physical activity and heritability have been well described. Nevertheless, there remains considerable unexplained variation in muscle mass and strength between older adults that may reflect not only the current rate of loss but the peak attained earlier in life. To date most epidemiological studies of sarcopenia have focused on factors modifying decline in later life; however, a life course approach to understanding sarcopenia, additionally, focuses on factors operating earlier in life including developmental influences. The epidemiological evidence linking low birth weight with lower muscle mass and strength is strong and consistent with replication in a number of different groups including children, young and older adults. However, most of the evidence for the cellular, hormonal, metabolic and molecular mechanisms underlying these associations comes from animal models. The next stage is to translate the understanding of mechanisms from animal muscle to human muscle enabling progress to be made not only in earlier identification of individuals at risk of sarcopenia but also in the development of beneficial interventions across the life course.

Keywords

agingdevelopmentepidemiologymechanismsarcopenia
Type
Reviews
Information
Journal of Developmental Origins of Health and Disease , Volume 1 , Issue 3 , June 2010 , pp. 150 - 157
Copyright
Copyright © Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1. Morley, JE, Baumgartner, RN, Roubenoff, R, et al. Sarcopenia. J Lab Clin Med. 2001; 137, 231–243.CrossRefGoogle ScholarPubMed
2. Sayer, AA, Syddall, HE, Martin, HJ, et al. Is grip strength associated with health-related quality of life? Findings from the Hertfordshire Cohort Study. Age Ageing. 2006; 35, 409–415.CrossRefGoogle ScholarPubMed
3. Sayer, AA, Dennison, EM, Syddall, HE, et al. Type 2 diabetes, muscle strength, and impaired physical function: the tip of the iceberg? Diabetes Care. 2005; 28, 2541–2542.CrossRefGoogle ScholarPubMed
4. Gale, CR, Martyn, CN, Cooper, C, Sayer, AA. Grip strength, body composition, and mortality. Int J Epidemiol. 2007; 36, 228–235.CrossRefGoogle ScholarPubMed
5. Janssen, I, Shepard, DS, Katzmarzyk, PT, Roubenoff, R. The healthcare costs of sarcopenia in the United States. J Am Geriatr Soc. 2004; 52, 80–85.CrossRefGoogle ScholarPubMed
6. Marcell, TJ. Sarcopenia: causes, consequences, and preventions. J Gerontol A Biol Sci Med Sci. 2003; 58, M911–M916.CrossRefGoogle ScholarPubMed
7. Roubenoff, R. Sarcopenia and its implications for the elderly. Eur J Clin Nutr. 2000; 54(Suppl 3), S40–S47.CrossRefGoogle ScholarPubMed
8. Arden, NK, Spector, TD. Genetic influences on muscle strength, lean body mass, and bone mineral density: a twin study. J Bone Miner Res. 1997; 12, 2076–2081.CrossRefGoogle ScholarPubMed
9. Vincent, KR, Braith, RW, Feldman, RA, et al. Resistance exercise and physical performance in adults aged 60 to 83. J Am Geriatr Soc. 2002; 50, 1100–1107.CrossRefGoogle ScholarPubMed
10. Skelton, DA, Young, A, Greig, CA, Malbut, KE. Effects of resistance training on strength, power, and selected functional abilities of women aged 75 and older. J Am Geriatr Soc. 1995; 43, 1081–1087.CrossRefGoogle Scholar
11. Liu, XG, Tan, LJ, Lei, SF, et al. Genome-wide association and replication studies identified TRHR as an important gene for lean body mass. Am J Hum Genet. 2009; 84, 418–423.CrossRefGoogle ScholarPubMed
12. Barker, DJP, Osmond, C, Forsen, T, Kajantie, E, Eriksson, J. Trajectories of growth among children who have coronary events as adults. N Engl J Med. 2005; 353, 1802–1809.CrossRefGoogle ScholarPubMed
13. Roseboom, T, de Rooij, S, Painter, R. The Dutch famine and its long-term consequences for adult health. Early Hum Dev. 2006; 82, 485–491.CrossRefGoogle ScholarPubMed
14. Lumey, LH, Stein, AD, Kahn, HS, et al. Cohort profile: the Dutch hunger winter families study. Int J Epidemiol. 2007; 36, 1196–1204.CrossRefGoogle ScholarPubMed
15. Lucas, A. Programming by early nutrition in man. In The Childhood Environment and Adult Disease. Ciba Foundation Symposium 156. (eds. Bock GR, Whelan J) 1991; pp. 38–50. John Wiley, Chichester, UK.Google Scholar
16. Gluckman, PD, Hanson, MA. Living with the past: evolution, development, and patterns of disease. Science. 2004; 305, 1733–1736.CrossRefGoogle ScholarPubMed
17. West-Eberhard, MJ. Phenotypic plasticity and the origins of diversity. Annu Rev Ecol Syst. 1989; 20, 249–278.CrossRefGoogle Scholar
18. Bateson, P, Barker, D, Clutton-Brock, T, et al. Developmental plasticity and human health. Nature. 2004; 430, 419–421.CrossRefGoogle ScholarPubMed
19. Gluckman, PD, Hanson, MA, Bateson, P, et al. Towards a new developmental synthesis: adaptive developmental plasticity and human disease. Lancet. 2009; 373, 1654–1657.CrossRefGoogle ScholarPubMed
20. Burdge, GC, Hanson, MA, Slater-Jefferies, JL, Lillycrop, KA. Epigenetic regulation of transcription: a mechanism for inducing variations in phenotype (foetal programming) by differences in nutrition during early life? Br J Nutr. 2007; 97, 1036–1046.CrossRefGoogle ScholarPubMed
21. Bergmann, RL, Bergmann, KE, Dudenhausen, JW. Undernutrition and growth restriction in pregnancy. Nestle Nutr Workshop Ser Pediatr Program. 2008; 61, 103–121.CrossRefGoogle ScholarPubMed
22. Sayer, AA, Cooper, C, Evans, JR, et al. Are rates of ageing determined in utero? Age Ageing. 1998; 27, 579–583.CrossRefGoogle ScholarPubMed
23. Sayer, AA, Syddall, HE, Gilbody, HJ, Dennison, EM, Cooper, C. Does sarcopenia originate in early life? Findings from the Hertfordshire Cohort Study. J Gerontol. 2004; 59A, 930–934.CrossRefGoogle Scholar
24. Kuh, D, Hardy, R, Butterworth, S, et al. Developmental origins of midlife grip strength: findings from a birth cohort study. J Gerontol A Biol Sci Med Sci. 2006; 61, 702–706.CrossRefGoogle ScholarPubMed
25. Inskip, HM, Godfrey, KM, Martin, HJ, et al. Size at birth and its relation to muscle strength in young adult women. J Int Med. 2007; 262, 368–374.CrossRefGoogle ScholarPubMed
26. Wadsworth, M, Kuh, D, Richards, M, Hardy, R. Cohort profile: the 1946 National Birth Cohort (MRC National Survey of Health and Development). Int J Epidemiol. 2006; 35, 49–54.CrossRefGoogle ScholarPubMed
27. Kuh, D, Hardy, R, Butterworth, S, et al. Developmental origins of midlife grip strength: findings from a birth cohort study. J Gerontol A Biol Sci Med Sci. 2006; 61, 702–706.CrossRefGoogle ScholarPubMed
28. Sayer, AA, Syddall, H, Martin, H, et al. The developmental origins of sarcopenia. J Nutr Health Aging. 2008; 12, 427–432.CrossRefGoogle ScholarPubMed
29. Sayer, AA, Syddall, HE, Dennison, EM, et al. Birth weight, weight at one year and body composition in older men: findings from the Hertfordshire Cohort Study. Am J Clin Nutr. 2004; 80, 199–203.CrossRefGoogle Scholar
30. Phillips, DIW. Relation of foetal growth to adult muscle mass and glucose tolerance. Diabet Med. 1995; 12, 686–690.CrossRefGoogle ScholarPubMed
31. Gale, CR, Martyn, CN, Kellingray, S, Eastell, R, Cooper, C. Intrauterine programming of adult body composition. J Clin Endocrinol Metab. 2001; 86, 267–272.Google ScholarPubMed
32. Yliharsila, H, Kajantie, E, Osmond, C, et al. Birth size, adult body composition and muscle strength in later life. Int J Obes (Lond). 2007; 31, 1392–1399.CrossRefGoogle ScholarPubMed
33. Hediger, ML, Overpeck, MD, Kuczmarski, RJ, et al. Muscularity and fatness of infants and young children born small or large-for-gestational-age. Pediatrics. 1998; 102, E60.CrossRefGoogle ScholarPubMed
34. Singhal, A, Wells, J, Cole, TJ, Fewtrell, M, Lucas, A. Programming of lean body mass: a link between birth weight, obesity, and cardiovascular disease? Am J Clin Nutr. 2003; 77, 726–730.CrossRefGoogle Scholar
35. Kahn, HS, Narayan, KM, Williamson, DF, Valdez, R. Relation of birth weight to lean and fat thigh tissue in young men. Int J Obes Relat Metab Disord. 2000; 24, 667–672.CrossRefGoogle ScholarPubMed
36. Sayer, AA, Dennison, EM, Syddall, HE, et al. The developmental origins of sarcopenia: using peripheral quantitative computed tomography to assess muscle size in older people. J Gerontol A Biol Sci Med Sci. 2008; 63, 835–840.CrossRefGoogle ScholarPubMed
37. Inskip, HM, Godfrey, KM, Robinson, SM, et al. Cohort profile: The Southampton Women’s Survey. Int J Epidemiol. 2006; 35, 42–48.CrossRefGoogle ScholarPubMed
38. Harvey, NC, Poole, JR, Javaid, MK, et al. Parental determinants of neonatal body composition. J Clin Endocrinol Metab. 2007; 92, 523–526.CrossRefGoogle ScholarPubMed
39. Dauncey, MJ, Gilmour, RS. Regulatory factors in the control of muscle development. Proc Nutr Soc. 1996; 55, 543–559.CrossRefGoogle ScholarPubMed
40. Lexell, J, Sjostrom, M, Nordlund, AS, Taylor, CC. Growth and development of human muscle: a quantitative morphological study of whole vastus lateralis from childhood to adult age. Muscle Nerve. 1992; 15, 404–409.CrossRefGoogle ScholarPubMed
41. Elder, GC, Kakulas, BA. Histochemical and contractile property changes during human muscle development. Muscle Nerve. 1993; 16, 1246–1253.CrossRefGoogle ScholarPubMed
42. Alessandri, G, Pagano, S, Bez, A, et al. Isolation and culture of human muscle-derived stem cells able to differentiate into myogenic and neurogenic cell lineages. Lancet. 2004; 364, 1872–1883.CrossRefGoogle ScholarPubMed
43. Maltin, CA, Delday, MI, Sinclair, KD, Steven, J, Sneddon, AA. Impact of manipulations of myogenesis in utero on the performance of adult skeletal muscle. Reproduction. 2001; 122, 359–374.CrossRefGoogle ScholarPubMed
44. Costello, PM, Rowlerson, A, Astaman, NA, et al. Peri-implantation and late gestation maternal undernutrition differentially affect foetal sheep skeletal muscle development. J Physiol. 2008; 586, 2371–2379.CrossRefGoogle ScholarPubMed
45. Greenwood, PL, Hunt, AS, Hermanson, JW, Bell, AW. Effects of birth weight and postnatal nutrition on neonatal sheep: II. Skeletal muscle growth and development. J Anim Sci. 2000; 78, 50–61.CrossRefGoogle ScholarPubMed
46. Dwyer, CM, Stickland, NC, Fletcher, JM. The influence of maternal nutrition on muscle fibre number development in the porcine foetus and on subsequent postnatal growth. J Anim Sci. 1994; 72, 911–917.CrossRefGoogle ScholarPubMed
47. Dwyer, CM, Madgwick, AJ, Ward, SS, Stickland, NC. Effect of maternal undernutrition in early gestation on the development of foetal myofibres in the guinea-pig. Reprod Fertil Dev. 1995; 7, 1285–1292.CrossRefGoogle ScholarPubMed
48. Wilson, SJ, Ross, JJ, Harris, AJ. A critical period for formation of secondary myotubes defined by prenatal undernourishment in rats. Development. 1988; 102, 815–821.CrossRefGoogle ScholarPubMed
49. Prakash, YS, Fournier, M, Sieck, GC. Effects of prenatal undernutrition on developing rat diaphragm. J Appl Physiol. 1993; 75, 1044–1052.CrossRefGoogle ScholarPubMed
50. Pond, WG, Yen, JT, Mersmann, HJ, Maurer, RR. Reduced mature size in progeny of swine severely restricted in protein intake during pregnancy. Growth Dev Aging. 1990; 54, 77–84.Google ScholarPubMed
51. Aihie Sayer, A, Cooper, C. Early undernutrition: good or bad for longevity?. In Handbook of Nutrition in the Aged, 3rd edn (ed. Watson RR), 2000; pp. 97–106. CRC Press Inc, Boca Raton, FL, USA.Google Scholar
52. Petry, CJ, Ozanne, SE, Hales, CN. Programming of intermediary metabolism. Mol Cell Endocrinol. 2001; 185, 81–91.CrossRefGoogle ScholarPubMed
53. Ozanne, SE, Wang, CL, Dorling, MW, Petry, CJ. Dissection of the metabolic actions of insulin in adipocytes from early growth-retarded male rats. J Endocrinol. 1999; 162, 313–319.CrossRefGoogle ScholarPubMed
54. Ozanne, SE, Smith, GD, Tikerpae, J, Hales, CN. Altered regulation of hepatic glucose output in the male offspring of protein-malnourished rat dams. Am J Physiol. 1996; 270, E559–E564.Google ScholarPubMed
55. Brameld, JM, Mostyn, A, Dandrea, J, et al. Maternal nutrition alters the expression of insulin-like growth factors in foetal sheep liver and skeletal muscle. J Endocrinol. 2000; 167, 429–437.CrossRefGoogle ScholarPubMed
56. Heasman, L, Brameld, J, Mostvn, A, et al. Maternal nutrient restriction during early to mid gestation alters the relationship between insulin-like growth factor I and bodyweight at term in foetal sheep. Reprod Fertil Dev. 2000; 12, 345–350.CrossRefGoogle Scholar
57. Tisi, DK, Liu, XJ, Wykes, LJ, Skinner, CD, Koski, KG. Insulin-like growth factor II and binding proteins 1 and 3 from second trimester human amniotic fluid are associated with infant birth weight. J Nutr. 2005; 135, 1667–1672.CrossRefGoogle ScholarPubMed
58. Ogilvy-Stuart, AL, Hands, SJ, Adcock, CJ, et al. Insulin, insulin-like growth factor I (IGF-I), IGF-binding protein-1, growth hormone, and feeding in the newborn. J Clin Endocrinol Metab. 1998; 83, 3550–3557.CrossRefGoogle ScholarPubMed
59. Rehfeldt, C, Kuhn, G. Consequences of birth weight for postnatal growth performance and carcass quality in pigs as related to myogenesis. J Anim Sci. 2006; 84(Suppl), E113–E123.CrossRefGoogle ScholarPubMed
60. Tilley, RE, McNeil, CJ, Ashworth, CJ, Page, KR, McArdle, HJ. Altered muscle development and expression of the insulin-like growth factor system in growth retarded foetal pigs. Domest Anim Endocrinol. 2007; 32, 167–177.CrossRefGoogle Scholar
61. Frampton, RJ, Jonas, HA, Larkins, RG. Increased secretion of insulin-like growth factor-binding proteins and decreased secretion of insulin-like growth factor-II by muscle from growth-retarded neonatal rats. J Endocrinol. 1991; 130, 33–42.CrossRefGoogle ScholarPubMed
62. Greenwood, PL, Bell, AW. Consequences of intra-uterine growth retardation for postnatal growth, metabolism and pathophysiology. Reprod Suppl. 2003; 61, 195–206.Google ScholarPubMed
63. Wang, J, Chen, L, Li, D, et al. Intrauterine growth restriction affects the proteomes of the small intestine, liver, and skeletal muscle in newborn pigs. J Nutr. 2008; 138, 60–66.CrossRefGoogle ScholarPubMed
64. Ozanne, SE, Olsen, GS, Hansen, LL, et al. Early growth restriction leads to down regulation of protein kinase C zeta and insulin resistance in skeletal muscle. J Endocrinol. 2003; 177, 235–241.CrossRefGoogle ScholarPubMed
65. Haddad, F, Adams, GR. Aging-sensitive cellular and molecular mechanisms associated with skeletal muscle hypertrophy. J Appl Physiol. 2006; 100, 1188–1203.CrossRefGoogle ScholarPubMed
66. Kandel, ES, Hay, N. The regulation and activities of the multifunctional serine/threonine kinase Akt/PKB. Exp Cell Res. 1999; 253, 210–229.CrossRefGoogle ScholarPubMed
67. Saini, A, Al-Shanti, N, Stewart, CE. Waste management – cytokines, growth factors and cachexia. Cytokine Growth Factor Rev. 2006; 17, 475–486.CrossRefGoogle ScholarPubMed
68. Bodine, SC, Stitt, TN, Gonzalez, M, et al. Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat Cell Biol. 2001; 3, 1014–1019.CrossRefGoogle ScholarPubMed
69. Raychaudhuri, N, Raychaudhuri, S, Thamotharan, M, Devaskar, SU. Histone code modifications repress glucose transporter 4 expression in the intrauterine growth-restricted offspring. J Biol Chem. 2008; 283, 13611–13626.CrossRefGoogle ScholarPubMed
70. Fulco, M, Cen, Y, Zhao, P, et al. Glucose restriction inhibits skeletal myoblast differentiation by activating SIRT1 through AMPK-mediated regulation of Nampt. Dev Cell. 2008; 14, 661–673.CrossRefGoogle ScholarPubMed
71. Moynihan, KA, Grimm, AA, Plueger, MM, et al. Increased dosage of mammalian Sir2 in pancreatic beta cells enhances glucose-stimulated insulin secretion in mice. Cell Metab. 2005; 2, 105–117.CrossRefGoogle ScholarPubMed
72. Bordone, L, Motta, MC, Picard, F, et al. Sirt1 regulates insulin secretion by repressing UCP2 in pancreatic beta cells. PLoS Biol. 2006; 4, e31.CrossRefGoogle ScholarPubMed
73. Fulco, M, Schiltz, RL, Iezzi, S, et al. Sir2 regulates skeletal muscle differentiation as a potential sensor of the redox state. Mol Cell. 2003; 12, 51–62.CrossRefGoogle ScholarPubMed
74. Chen, D, Steele, AD, Lindquist, S, Guarente, L. Increase in activity during calorie restriction requires Sirt1. Science. 2005; 310, 1641.CrossRefGoogle ScholarPubMed
75. Thompson, CH, Sanderson, AL, Sandeman, D, et al. Foetal growth and insulin resistance in adult life: role of skeletal muscle morphology. Clin Sci (Colch). 1997; 92, 291–296.CrossRefGoogle ScholarPubMed
76. Jensen, CB, Storgaard, H, Madsbad, S, Richter, EA, Vaag, AA. Altered skeletal muscle fibre composition and size precede whole-body insulin resistance in young men with low birth weight. J Clin Endocrinol Metab. 2007; 92, 1530–1534.CrossRefGoogle ScholarPubMed
77. Jensen, CB, Martin-Gronert, MS, Storgaard, H, et al. Altered PI3-kinase/Akt signalling in skeletal muscle of young men with low birth weight. PLoS One. 2008; 3, e3738.CrossRefGoogle ScholarPubMed
78. Aihie Sayer, A, Cooper, C. Aging, sarcopenia and the life course. Rev Clin Gerontol. 2007; 16, 265–274.CrossRefGoogle Scholar