Abstract
Obesity is a major public health problem. The population is growing older, and the prevalence of obesity in the elderly is rising. In normal aging, changes in the body composition occur that result in a shift toward decreased muscle mass and increased fat mass. This age-related progressive loss of muscle mass and strength is called sarcopenia. Sarcopenic obesity, which describes the process of muscle loss combined with increased body fat as people age, is associated with loss of strength and function, reduced quality of life, and even mortality. The pathogenesis of sarcopenic obesity is complex and involves multiple interactions between lifestyle, endocrine, and immunological factors. Recent epidemiological studies suggest that sarcopenic obesity is related to accelerated functional decline and high risk of diseases and mortality and, therefore, the identification of affected older patients should be an essential goal of clinicians. This paper addresses the definition and epidemiology of sarcopenic obesity and its underlying pathophysiology. In addition, this article describes the clinical significance and management strategies of sarcopenic obesity.
References
2. Mokdad AH, Bowman BA, Ford ES, Vinicor F, Marks JS, Koplan JP. The continuing epidemics of obesity and diabetes in the United States. JAMA. 2001; 286:1195–200.
3. Newman AB, Lee JS, Visser M, Goodpaster BH, Kritchevsky SB, Tylavsky FA, Nevitt M, Harris TB. Weight change and the conservation of lean mass in old age: the Health, Aging and Body Composition Study. Am J Clin Nutr. 2005; 82:872–8.
4. Schrager MA, Metter EJ, Simonsick E, Ble A, Bandinelli S, Lauretani F, Ferrucci L. Sarcopenic obesity and inflammation in the InCHIANTI study. J Appl Physiol (1985). 2007; 102:919–25.
6. Hughes VA, Frontera WR, Wood M, Evans WJ, Dallal GE, Roubenoff R, Fiatarone Singh MA. Longitudinal muscle strength changes in older adults: influence of muscle mass, physical activity, and health. J Gerontol A Biol Sci Med Sci. 2001; 56:B209–17.
7. Goodpaster BH, Park SW, Harris TB, Kritchevsky SB, Nevitt M, Schwartz AV, Simonsick EM, Tylavsky FA, Visser M, Newman AB. The loss of skeletal muscle strength, mass, and quality in older adults: the health, aging and body composition study. J Gerontol A Biol Sci Med Sci. 2006; 61:1059–64.
9. Solomon AM, Bouloux PM. Modifying muscle mass – the endocrine perspective. J Endocrinol. 2006; 191:349–60.
10. Dreyer HC, Volpi E. Role of protein and amino acids in the pathophysiology and treatment of sarcopenia. J Am Coll Nutr. 2005; 24:140S–145S.
11. Szulc P, Duboeuf F, Marchand F, Delmas PD. Hormonal and lifestyle determinants of appendicular skeletal muscle mass in men: the MINOS study. Am J Clin Nutr. 2004; 80:496–503.
12. Roth SM, Metter EJ, Ling S, Ferrucci L. Inflammatory factors in age-related muscle wasting. Curr Opin Rheumatol. 2006; 18:625–30.
14. Marcell TJ. Sarcopenia: causes, consequences, and preventions. J Gerontol A Biol Sci Med Sci. 2003; 58:M911–6.
15. Statistics Korea. Population Projections (2010∼2060) and various population-related indicators (birth rate, death rate and life expectancy) on the basis of the results from the 2010 Population Census [Internet]. Daejeon: Statistics Korea; [cited 2013 12 15]. Available from:. http://www.index.go.kr/egams/stts/jsp/potal/stts/PO_STTS_IdxMain.jsp?idx_cd=1009&bbs=INDX_001.
16. Abellan van Kan G. Epidemiology and consequences of sarcopenia. J Nutr Health Aging. 2009; 13:708–12.
17. Stenholm S, Harris TB, Rantanen T, Visser M, Kritchevsky SB, Ferrucci L. Sarcopenic obesity: definition, cause and consequences. Curr Opin Clin Nutr Metab Care. 2008; 11:693–700.
18. Baumgartner RN, Koehler KM, Gallagher D, Romero L, Heymsfield SB, Ross RR, Garry PJ, Lindeman RD. Epidemiology of sarcopenia among the elderly in New Mexico. Am J Epidemiol. 1998; 147:755–63.
20. Davison KK, Ford ES, Cogswell ME, Dietz WH. Percentage of body fat and body mass index are associated with mobility limitations in people aged 70 and older from NHANES III. J Am Geriatr Soc. 2002; 50:1802–9.
21. Zoico E, Di Francesco V, Guralnik JM, Mazzali G, Bortolani A, Guariento S, Sergi G, Bosello O, Zamboni M. Physical disability and muscular strength in relation to obesity and different body composition indexes in a sample of healthy elderly women. Int J Obes Relat Metab Disord. 2004; 28:234–41.
22. Newman AB, Kupelian V, Visser M, Simonsick E, Goodpaster B, Nevitt M, Kritchevsky SB, Tylavsky FA, Rubin SM, Harris TB. Health ABC Study Investigators. Sarcopenia: alternative definitions and associations with lower extremity function. J Am Geriatr Soc. 2003; 51:1602–9.
23. Kim TN, Yang SJ, Yoo HJ, Lim KI, Kang HJ, Song W, Seo JA, Kim SG, Kim NH, Baik SH, Choi DS, Choi KM. Prevalence of sarcopenia and sarcopenic obesity in Korean adults: the Korean sarcopenic obesity study. Int J Obes (Lond). 2009; 33:885–92.
24. Janssen I, Heymsfield SB, Ross R. Low relative skeletal muscle mass (sarcopenia) in older persons is associated with functional impairment and physical disability. J Am Geriatr Soc. 2002; 50:889–96.
25. Janssen I, Baumgartner RN, Ross R, Rosenberg IH, Roubenoff R. Skeletal muscle cutpoints associated with elevated physical disability risk in older men and women. Am J Epidemiol. 2004; 159:413–21.
26. Kim TN, Park MS, Lim KI, Yang SJ, Yoo HJ, Kang HJ, Song W, Seo JA, Kim SG, Kim NH, Baik SH, Choi DS, Choi KM. Skeletal muscle mass to visceral fat area ratio is associated with metabolic syndrome and arterial stiffness: The Korean Sarcopenic Obesity Study (KSOS). Diabetes Res Clin Pract. 2011; 93:285–91.
27. Bastard JP, Maachi M, Lagathu C, Kim MJ, Caron M, Vidal H, Capeau J, Feve B. Recent advances in the relationship between obesity, inflammation, and insulin resistance. Eur Cytokine Netw. 2006; 17:4–12.
28. Dyck DJ, Heigenhauser GJ, Bruce CR. The role of adipokines as regulators of skeletal muscle fatty acid metabolism and insulin sensitivity. Acta Physiol (Oxf). 2006; 186:5–16.
29. Goodpaster BH, Krishnaswami S, Resnick H, Kelley DE, Haggerty C, Harris TB, Schwartz AV, Kritchevsky S, Newman AB. Association between regional adipose tissue distribution and both type 2 diabetes and impaired glucose tolerance in elderly men and women. Diabetes Care. 2003; 26:372–9.
30. Goodpaster BH, Thaete FL, Kelley DE. Thigh adipose tissue distribution is associated with insulin resistance in obesity and in type 2 diabetes mellitus. Am J Clin Nutr. 2000; 71:885–92.
31. Goodpaster BH, Brown NF. Skeletal muscle lipid and its association with insulin resistance: what is the role for exercise? Exerc Sport Sci Rev. 2005; 33:150–4.
32. van Loon LJ, Goodpaster BH. Increased intramuscular lipid storage in the insulin-resistant and endurance-trained state. Pflugers Arch. 2006; 451:606–16.
33. Weltman A, Weltman JY, Veldhuis JD, Hartman ML. Body composition, physical exercise, growth hormone and obesity. Eat Weight Disord. 2001; 6(3 Suppl):28–37.
34. Van Dam PS, Smid HE, de Vries WR, Niesink M, Bolscher E, Waasdorp EJ, Dieguez C, Casanueva FF, Koppeschaar HP. Reduction of free fatty acids by acipimox enhances the growth hormone (GH) responses to GH-releasing peptide 2 in elderly men. J Clin Endocrinol Metab. 2000; 85:4706–11.
35. Waters DL, Qualls CR, Dorin RI, Veldhuis JD, Baumgartner RN. Altered growth hormone, cortisol, and leptin secretion in healthy elderly persons with sarcopenia and mixed body composition phenotypes. J Gerontol A Biol Sci Med Sci. 2008; 63:536–41.
36. Allan CA, Strauss BJ, McLachlan RI. Body composition, metabolic syndrome and testosterone in ageing men. Int J Impot Res. 2007; 19:448–57.
37. Cappola AR, Bandeen-Roche K, Wand GS, Volpato S, Fried LP. Association of IGF-I levels with muscle strength and mobility in older women. J Clin Endocrinol Metab. 2001; 86:4139–46.
38. Schaap LA, Pluijm SM, Smit JH, van Schoor NM, Visser M, Gooren LJ, Lips P. The association of sex hormone levels with poor mobility, low muscle strength and incidence of falls among older men and women. Clin Endocrinol (Oxf). 2005; 63:152–60.
39. LaMonte MJ, Blair SN. Physical activity, cardiorespiratory fitness, and adiposity: contributions to disease risk. Curr Opin Clin Nutr Metab Care. 2006; 9:540–6.
41. Flegal KM, Kit BK, Orpana H, Graubard BI. Association of all-cause mortality with overweight and obesity using standard body mass index categories: a systematic review and metaanalysis. JAMA. 2013; 309:71–82.
42. Zamboni M, Mazzali G, Fantin F, Rossi A, Di Francesco V. Sarcopenic obesity: a new category of obesity in the elderly. Nutr Metab Cardiovasc Dis. 2008; 18:388–95.
43. Baumgartner RN, Wayne SJ, Waters DL, Janssen I, Gallagher D, Morley JE. Sarcopenic obesity predicts instrumental activities of daily living disability in the elderly. Obes Res. 2004; 12:1995–2004.
44. Aubertin-Leheudre M, Lord C, Goulet ED, Khalil A, Dionne IJ. Effect of sarcopenia on cardiovascular disease risk factors in obese postmenopausal women. Obesity (Silver Spring). 2006; 14:2277–83.
45. Borst SE. Interventions for sarcopenia and muscle weakness in older people. Age Ageing. 2004; 33:548–55.
46. Adamo ML, Farrar RP. Resistance training, and IGF involvement in the maintenance of muscle mass during the aging process. Ageing Res Rev. 2006; 5:310–31.
47. Fiatarone MA, O'Neill EF, Ryan ND, Clements KM, Solares GR, Nelson ME, Roberts SB, Kehayias JJ, Lipsitz LA, Evans WJ. Exercise training and nutritional supplementation for physical frailty in very elderly people. N Engl J Med. 1994; 330:1769–75.
48. Marzetti E, Leeuwenburgh C. Skeletal muscle apoptosis, sarcopenia and frailty at old age. Exp Gerontol. 2006; 41:1234–8.
49. Mazzali G, Di Francesco V, Zoico E, Fantin F, Zamboni G, Benati C, Bambara V, Negri M, Bosello O, Zamboni M. Interrelations between fat distribution, muscle lipid content, adipocytokines, and insulin resistance: effect of moderate weight loss in older women. Am J Clin Nutr. 2006; 84:1193–9.
50. Solerte SB, Gazzaruso C, Bonacasa R, Rondanelli M, Zamboni M, Basso C, Locatelli E, Schifino N, Giustina A, Fioravanti M. Nutritional supplements with oral amino acid mixtures increases whole-body lean mass and insulin sensitivity in elderly subjects with sarcopenia. Am J Cardiol. 2008; 101(11A):69E–77E.
Table 1.
Measuring techniques | Definition of sarcopenia (cut-off value) | Definition of obesity (cut-off value) | Mean age (SD) | Prevalence (%) | |
---|---|---|---|---|---|
New Mexico Aging Process Study (Baumgartner et al.) [19] | DXA | ASM/height2 −2SD below mean of young population (< 7.26 kg/m² in men and < 5.45 kg/m² in women) | Body fat percentage greater than median (> 27% in men and 38% in women) | 60 and over | M: 4.4 F: 3.0 |
NHANES III (Davison et al.) [20] | BIA | Two lower quintiles of total skeletal muscle mass/height² (< 9.12 kg/m² in men and < 6.53 kg/m² in women) | Two highest quintiles of body fat percentage (> 27% in men and 38% in women) | M: 76.3 (1.7a) F: 77.3 (2.2a) | M: 9.6 F:7.4 |
Community-dwelling older people in Verona (Zoico et al.) [21] | DXA | Two lower quintiles of ASM/height² (< 5.7 kg/m² in women) | Two highest quintiles of body fat percentage (> 42.9% in women) | F:71.7 (2.4) | F: 12.4 |
Korean Sarcopenic Obesity Study (Kim et al.) [23, 26] | DXA | SMI −2SD below mean of young population (< 7.26 kg/m² in men and < 5.45 kg/m² in women) | Two highest quintiles of body fat percentage (> 27% in men and 38% in women) | 60 and over | M: 5.1 F: 12.5 |
DXA and CT | MFR: ASM/VFA |
Adapted from Curr Opin Clin Nutr Metab Care 2008;11:693–700 [17] ASM, appendicular skeletal muscle mass; BIA, bioelectric impedence analysis; CT, computed tomography; DXA, dual energy X-ray absorptiometry; F, female; M, male; MFR, muscle-to-fat ratio; SMI, skeletal muscle index (total skeletal muscle mass (kg)/weight (kg) × 100); VFA, visceral fat area.