Sarcopenic obesity: Definition, cause and consequences

Current Opinion in Clinical Nutrition and Metabolic Care

Volumn 11, Issue 6, 2008, Pages 693-700

  Stenholm, Sari ^a,b   Harris, Tamara B ^a   Rantanen, Taina ^c   Visser, Marjolein ^d,e   Kritchevsky, Stephen B ^f   Ferrucci, Luigi ^a  

^a NATIONAL INSTITUTE ON AGING   (United States)

^b NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

^c UNIVERSITY OF JYVÄSKYLÄ   (Finland)

^d VU UNIVERSITY AMSTERDAM   (Netherlands)

^e VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^f WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

Adipose tissue; Body composition; Disability; Muscle strength; Obesity; Older people; Sarcopenia

Indexed keywords

CYTOKINE; GROWTH HORMONE; INSULIN; TESTOSTERONE;

AGING; BODY COMPOSITION; CALORIC INTAKE; DISEASE ASSOCIATION; FUNCTIONAL DISEASE; HORMONE ACTION; HORMONE RELEASE; HUMAN; IMMOBILIZATION; INFLAMMATION; INSULIN RESISTANCE; MALNUTRITION; MORTALITY; MUSCLE ATROPHY; MUSCLE MASS; MUSCLE STRENGTH; MUSCLE WEAKNESS; OBESITY; PATHOPHYSIOLOGY; PHYSICAL ACTIVITY; PREVALENCE; REVIEW; RISK FACTOR; SARCOPENIC OBESITY; WEIGHT REDUCTION;

AGED; AGING; COMORBIDITY; EXERCISE; FEMALE; HEALTH STATUS; HUMANS; MALE; MUSCLE STRENGTH; MUSCLE, SKELETAL; MUSCULAR ATROPHY; OBESITY; RISK FACTORS;

EID: 55149101319     PISSN: 13631950     EISSN: 15353885     Source Type: Journal    
DOI: 10.1097/MCO.0b013e328312c37d     Document Type: Review

References (109)

1. Baumgartner RN. Body composition in healthy aging. Ann N Y Acad Sci 2000; 904:437-448.
2. Zamboni M, Mazzali G, Fantin F, et al. Sarcopenic obesity: a new category of obesity in the elderly. Nutr Metab Cardiovasc Dis 2008; 18:388-395. Review article in which authors discuss about definition, pathogenesis, clinical implications and treatment of sarcopenic obesity.
3. Russo CR, Ricca M, Ferrucci L. True osteoporosis and frailty-related osteopenia: two different clinical entities. J Am Geriatr Soc 2000; 48:1738-1739.
4. Maggi S, Lauretani F, Ferrucci L, et al. The quality of bone: a 'magic natural alloy'. Aging Clin Exp Res 2004; 16 (Suppl 3):3-9.
5. WHO. Obesity: preventing and managing the global epidemic. Report of a WHO Consultation. Geneva, Switzerland: WHO; 2000. WHO Technical Report Series 894.
6. Rosenberg IH. Sarcopenia: origins and clinical relevance. J Nutr 1997; 127:9903-9915.
7. Marcell TJ. Sarcopenia: causes, consequences, and preventions. J Gerontol A Biol Sci Med Sci 2003; 58:M911-M916.
8. Thomas DR. Loss of skeletal muscle mass in aging: examining the relationship of starvation, Sarcopenia and cachexia. Clin Nutr 2007; 26:389-399.
9. Rosenberg I. Epidemiologic and methodologic problems in determining nutritional status of older persons. Am J Clin Nutr 1989; 50:1131-1133.
10. Doherty TJ, Vandervoort AA, Brown WF. Effects of ageing on the motor unit: a brief review. Can J Appl Physiol 1993; 18:331-358.
11. Campbell MJ, McComas AJ, Petito F. Physiological changes in ageing muscles. J Neural Neurosurg Psychiatry 1973; 36:174-182.
12. Baumgartner R, Koehler K, Gallagher D, et al. Epidemiology of Sarcopenia among the elderly in New Mexico. Am J Epidemiol 1998; 147:755-763.
13. Janssen I, Heymsfield SB, Ross R, et al. Low relative skeletal muscle mass (sarcopenia) in older persons is associated with functional impairment and physical disability. J Am Geriatr Soc 2002; 50:889-896.
14. Newman AB, Kupelian V, Visser M, et al. Sarcopenia: alternative definitions and associations with lower extremity function. J Am Geriatr Soc 2003; 51:1602-1609.
15. Lauretani F, Russo C, Bandinelli S, et al. Age-associated changes in skeletal muscles and their effect on mobility: an operational diagnosis of sarcopenia. J Appl Physiol 2003; 95:1851-1860.
16. Goodpaster BH, Park SW, Harris TB, et al. 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; 61A:M1059-M1064.
17. Hughes VA, Frontera WR, Wood M, et al. 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-B217.
18. Lexell J, Taylor CC, Sjöström M. What is the cause of the ageing atrophy? Total number, size and proportion of different fiber types studied in whole vastus lateralis muscle from 15- to 83-year-old men. J Neural Sci 1988; 84:275-294.
19. Larsson L, Li X, Frontera WR. Effects of aging on shortening velocity and myosin isoform composition in single human skeletal muscle cells. Am J Physiol 1997; 272:C638-C649.
20. Sipilä S, Suominen H. Knee extension strength and walking speed in relation to quadriceps muscle composition and training in elderly women. Clin Physiol 1994; 14:433-442.
21. Goodpaster BH, Carlson CL, Visser M, et al. Attenuation of skeletal muscle and strength in the elderly; the Health ABC Study. J Appl Physiol 2001; 90:2157-2165.
22. Delbono O. Neural control of aging skeletal muscle. Aging Cell 2003; 2: 21-29.
23. Visser M, Newman AB, Nevitt MC, et al. Reexamining the sarcopenia hypothesis. Muscle mass versus muscle strength. Health, Aging, and Body Composition Study Research Group. Ann N Y Acad Sci 2000; 904:456-461.
24. Visser M, Goodpaster BH, Kritchevsky SB, et al. Muscle mass, muscle strength, and muscle fat infiltration as predictors of incident mobility limitations in well functioning older persons. J Gerontol A Biol Sci Med Sci 2005• 60:M324-M333.
25. Newman AB, Kupelian V, Visser M, et al. Strength, but not muscle mass, is associated with mortality in the health, aging and body composition study cohort. J Gerontol A Biol Sci Med Sci 2006; 61A:M72-M77.
26. NIH Consensus Development Panel on Osteoporosis Prevention, Diagnosis, and Therapy. Osteoporosis Prevention, Diagnosis, and Therapy. JAMA 2001; 285:785-795.
27. Dennison E, Cole Z, Cooper C. Diagnosis and epidemiology of Osteoporosis. Curr Opin Rheumatol 2005; 17:456-461.
28. Visser M, Deeg DJ, Lips P, et al. Skeletal muscle mass and muscle strength in relation to lower-extremity performance in older men and women. J Am Geriatr Soc 2000; 48:381-386.
29. Davison KK, Ford E, Cogswell M, Dietz W. 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; 50:1802-1809.
30. Zoico E, Di Francesco V, Guralnik JM, et al. Physical disability and muscular strength in relation to obesity and different body composition indexes in a sample of healthy elderly women, lnt J Obes Relat Metab Disord 2004; 28:234-241.
31. Schrager MA, Metter EJ, Simonsick E, et al. Sarcopenic obesity and inflammation in the InCHIANTI study. J Appl Physiol 2007; 102:919-925. Using cross-sectional data from InCHIANTI study, this study found that obesity directly affects inflammation, which in turn negatively affects muscle strength. This finding suggests that the role of inflammation may be important to the development and progression of sarcopenic obesity.
32. Stenholm S, Rantanen T, Heliövaara M, Koskinen S. The mediating role of C-reactive protein and handgrip strength between obesity and walking limitation. J Am Geriatr Soc 2008; 56:462-469. On the basis of the representative sample of older adults in Finland, this study found that combination of high fat percentage and low handgrip strength is associated with increased level of CRP as well as with walking limitation.
33. Shock NW, Greulich R, Andres R, et al. Normal human aging: the Baltimore Longitudinal Study of Aging. Washington, DC: U.S. Govt. Printing Office; 1984. NIH Publication 84-2450.
34. Aromaa A, Koskinen S. Health and functional capacity in Finland. Baseline results of the Health 2000 health examination survey. Helsinki: Publications of the National Public Health Institute B12/2004; 2004. http://www.ktl.fi/ terveys2000/index.uk.html.
35. Ferrucci L, Bandinelli S, Benvenuti E, et al. Subsystems contributing to the decline in ability to walk: bridging the gap between epidemiology and geriatric practice in the InCHIANTI study. J Am Geriatr Soc 2000; 48: 1618-1625.
36. Sonnenberg CM, Deeg DJ, Comijs HC, et al. Trends in antidepressant use in the older population: results from the LASA-study over a period of 10 years. J Affect Disord (in press). doi:10.1016/j.jad.2008.03.009.
37. Deeg DJ, van Tilburg T, Smit JH, de Leeuw ED. Attrition in the Longitudinal Aging Study Amsterdam. The effect of differential inclusion in side studies. J Clin Epidemiol 2002; 55:319-328.
38. Rissanen A, Heliövaara M, Aromaa A. Overweight and anthropometric changes in adulthood: a prospective study of 17000 Finns, Int J Obes 1988; 12:391-401.
39. Droyvold WB, Nilsen TI, Kruger O, et al. Change in height, weight and body mass index: longitudinal data from the HUNT Study in Norway, Int J Obes 2006; 30:935-939.
40. Ding J, Kritchevsky SB, Newman AB, et al. Effects of birth cohort and age on body composition in a sample of community-based elderly. Am J Clin Nutr 2007; 85:405-410.
41. Rantanen T, Masaki KT, Foley D, et al. Grip strength changes over 27 yr in Japanese-American men. J Appl Physiol 1998; 85:2047-2053.
42. Bassey EJ. Longitudinal changes in selected physical capabilities: muscle strength, flexibility and body size. Age Ageing 1998; 27:12-16.
43. Frontera WR, Hughes VA, Fielding RA, et al. Aging of skeletal muscle: a 12-yr longitudinal study. J Appl Physiol 2000; 88:1321-1326.
44. Beaufrere B, Morio B. Fat and protein redistribution with aging: metabolic considerations. Eur J Clin Nutr 2000; 54 (Suppl 3):S48-S53.
45. Enzi G, Gasparo M, Biondetti PR, et al. Subcutaneous and visceral fat distribution according to sex, age, and overweight, evaluated by computed tomography. Am J Clin Nutr 1986; 44:739-746.
46. Zamboni M, Armellini F, Harris T, et al. Effects of age on body fat distribution and cardiovascular risk factors in women. Am J Clin Nutr 1997; 66:111-115.
47. Horber FF, Gruber B, Thomi F, et al. Effect of sex and age on bone mass, body composition and fuel metabolism in humans. Nutrition 1997; 13:524-534.
48. Visser M, Kritchevsky SB, Goodpaster BH, et al. Leg muscle mass and composition in relation to lower extremity performance in men and women aged 70 to 79: the Health, Aging and Body Composition Study. J Am Geriatr Soc 2002; 50:897-904.
49. Elia M, Ritz P, Stubbs RJ. Total energy expenditure in the elderly. Eur J Clin Nutr 2000; 54:S92-S103.
50. Morley JE, Baumgartner RN, Roubenoff R, et al. Sarcopenia. J Lab Clin Med 2001; 137:231-243.
51. Doherty T. Aging and sarcopenia. J Appl Physiol 2003; 95:1717-1727.
52. Roubenoff R. Sarcopenia: effects on body composition and function. J Gerontol A Biol Sci Med Sci 2003; 58A:M1012-M1017.
53. LaMonte MJ, Blair SN. Physical activity, cardiorespiratory fitness, and adiposity: contributions to disease risk. Curr Opin Clin Nutr Metab Care 2006; 9:540-546.
54. Duvigneaud N, Matton L, Wijndaele K, et al. Relationship of obesity with physical activity, aerobic fitness and muscle strength in Flemish adults. J Sports Med Phys Fitness 2008; 48:201-210.
55. Wang X, Miller GD, Messier SP, Nicklas BJ. Knee strength maintained despite loss of lean body mass during weight loss in older obese adults with knee osteoarthritis. J Gerontol A Biol Sci Med Sci 2007; 62:866-871.
56. Frimel TN, Sinacore DR, Villareal DT. Exercise attenuates the weight-loss-induced reduction in muscle mass in frail obese older adults. Med Sci Sports Exerc 2008; 40:1213-1219. This randomized trial examined the effect of combined diet and exercise intervention on body composition and muscle strength among obese older people. During 6-month intervention, persons in the diet + exercise group lost fat mass but increased muscle strength indicating a tight connection between adiposity and muscle impairment.
57. Fantuzzi G. Adipose tissue, adipokines, and inflammation. J Allergy Clin Immunol 2005; 115:911-919; quiz 920.
58. Fontana L, Eagon JC, Trujillo ME, et al. Visceral fat adipokine secretion is associated with systemic inflammation in obese humans. Diabetes 2007; 56:1010-1013. This study is among the first studies to examine the adipokine production by visceral fat in obese participants. By examining blood samples from the portal vein and radial artery during open gastric bypass surgery, they were able to show that plasma IL-6 concentrations were much higher in portal vein than in peripheral artery blood in obese participants, demonstrating that visceral fat is an important source of IL-6 production in obese people.
59. Hung J, McQuillan BM, Thompson PL, Beilby JP. Circulating adiponectin levels associate with inflammatory markers, insulin resistance and metabolic syndrome independent of obesity, Int J Obes 2008; 32:772-779.
60. Visser M, Pahor M, Taaffe DR, et al. Relationship of interleukin-6 and tumor necrosis factor-α with muscle mass and muscle strength in elderly men and women: the Health ABC Study. J Gerontol A Biol Sci Med Sci 2002; 57A:M326-M332.
61. Cesari M, Kritchevsky SB, Baumgartner RN, et al. Sarcopenia, obesity, and inflammation - results from the Trial of Angiotensin Converting Enzyme Inhibition and Novel Cardiovascular Risk Factors study. Am J Clin Nutr 2005; 82:428-434.
62. Schaap LA, Pluijm SM, Deeg DJ, Visser M. Inflammatory markers and loss of muscle mass (sarcopenia) and strength. Am J Med 2006; 119:526.e529-526e.517.
63. Barbieri M, Ferrucci L, Ragno E, et al. Chronic inflammation and the effect of IGF-I on muscle strength and power in older persons. Am J Physiol Endocrinol Metab 2003; 284:E481-E487.
64. Roth SM, Metter EJ, Ling S, Ferrucci L. Inflammatory factors in age-related muscle wasting. Curr Opin Rheumatol 2006; 18:625-630.
65. Bastard JP, Maachi M, Lagathu C, et al. Recent advances in the relationship between obesity, inflammation, and insulin resistance. Eur Cytokine Netw 2006; 17:4-12.
66. 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.
67. Goodpaster BH, Brown NF. Skeletal muscle lipid and its association with insulin resistance: what is the role for exercise? Exerc Sport Sci Rev 2005; 33:150-154.
68. Kelley DE, Slasky BS, Janosky J. Skeletal muscle density: effects of obesity and noninsulin-dependent diabetes mellitus. Am J Clin Nutr 1991; 54:509-515.
69. Goodpaster BH, Krishnaswami S, Resnick H, et al. Association between regional adipose tissue distribution and both type 2 diabetes and impaired glucose tolerance in elderly men and women. Diabetes Care 2003; 26:372-379.
70. 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; 71:885-892.
71. van Loon LJ, Goodpaster BH. Increased intramuscular lipid storage in the insulin-resistant and endurance-trained state. Pflugers Arch 2006; 451: 606-616.
72. Biolo G, Declan Fleming RY, Wolfe RR. Physiologic hyperinsulinemia stimulates protein synthesis and enhances transport of selected amino acids in human skeletal muscle. J Clin Invest 1995; 95:811-819.
73. Fujita S, Rasmussen BB, Cadenas JG, et al. Effect of insulin on human skeletal muscle protein synthesis is modulated by insulin-induced changes in muscle blood flow and amino acid availability. Am J Physiol Endocrinol Metab 2006; 291:E745-E754.
74. Nomura T, Ikeda Y, Nakao S, et al. Muscle strength is a marker of insulin resistance in patients with type 2 diabetes: a pilot study. Endocr J 2007; 54:791-796.
75. Abbatecola AM, Ferrucci L, Ceda G, et al. Insulin resistance and muscle strength in older persons. J Gerontol A Biol Sci Med Sci 2005; 60A:1278-1282.
76. Guillet C, Boirie Y. Insulin resistance: a contributing factor to age-related muscle mass loss? Diabetes Metab 2005; 31. Spec No 2:5S20-25S26.
77. Park SW, Goodpaster BH, Strotmeyer ES, et al. Accelerated loss of skeletal muscle strength in older adults with type 2 diabetes: the health, aging, and body composition study. Diabetes Care 2007; 30:1507-1512. Based on 3-year follow-up of the Health ABC study, this is the first longitudinal study to show that type 2 diabetes is associated with accelerated loss of muscle strength and mass in older adults.
78. Eves ND, Plotnikoff RC. Resistance training and type 2 diabetes: considerations for implementation at the population level. Diabetes Care 2006; 29: 1933-1941.
79. Campbell PJ, Carlson MG, Nurjhan N. Fat metabolism in human obesity. Am J Physiol 1994; 266:E600-E605.
80. Petersen KF, Befroy D, Dufour S, et al. Mitochondrial dysfunction in the elderly: possible role in insulin resistance. Science 2003; 300:1140-1142.
81. Van Dam PS, Smid HE, de Vries WR, et al. 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; 85:4706-4711.
82. Weltman A, Weltman JY, Veldhuis JD, Hartman ML. Body composition, physical exercise, growth hormone and obesity. Eat Weight Disord 2001; 6:28-37.
83. Waters DL, Quails CR, Dorm RI, et al. 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; 63:536-541.
84. Allan CA, Strauss BJ, McLachlan RI. Body composition, metabolic syndrome and testosterone in ageing men. Int J Impot Res 2007; 19:448-457.
85. Ceda GP, Dall'Aglio E, Maggio M, et al. Clinical implications of the reduced activity of the GH-IGF-I axis in older men. J Endocrinol Invest 2005; 28:96-100.
86. Schaap LA, Pluijm SM, Smit JH, et al. The association of sex hormone levels with poor mobility, low muscle strength and incidence of falls among older men and women. Clin Endocrinol 2005; 63:152-160.
87. Cappola AR, Bandeen-Roche K, Wand GS, et al. Association of IGF-I levels with muscle strength and mobility in older women. J Clin Endocrinol Metab 2001; 86:4139-4146.
88. Chu LW, Tam S, Kung AW, et al. Serum total and bioavailable testosterone levels, central obesity, and muscle strength changes with aging in healthy Chinese men. J Am Geriatr Soc (in press). doi:10.1111/J.1532-5415.2008. 01746.x.
89. Morley JE. Anorexia of aging: physiologic and pathologic. Am J Clin Nutr 1997; 66:760-773.
90. Dreyer HC, Volpi E. Role of protein and amino acids in the pathophysiology and treatment of sarcopenia. J Am Coll Nutr 2005; 24:1403-1458.
91. Campbell WW, Leidy HJ. Dietary protein and resistance training effects on muscle and body composition in older persons. J Am Coll Nutr 2007; 26:6963-7033.
92. Houston DK, Nicklas BJ, Ding J, et al. Dietary protein intake is associated with lean mass change in older, community-dwelling adults: the Health, Aging, and Body Composition (Health ABC) Study. Am J Clin Nutr 2008; 87:150-155.
93. Houston DK, Stevens J, Cai J. Abdominal fat distribution and functional limitations and disability in a biracial cohort: the Atherosclerosis Risk in Communities Study, Int J Obes 2005; 29:1457-1463.
94. Alley DE, Chang VW. The changing relationship of obesity and disability, 1988-2004. JAMA 2007; 298:2020-2027. Using data from NHANES, this representative study shows that opposite to the decreased disability prevalence among nonobese, the obesity-associated disability has increased from 1988-1994 to 1999-2004.
95. Stenholm S, Sainio P, Rantanen T, et al. Effect of co-morbidity on the association of high body mass index with walking limitation among men and women aged 55 years and older. Aging Clin Exp Res 2007; 19:277-283.
96. Rantanen T, Harris T, Leveille SG, et al. Muscle strength and body mass index as long-term predictors of mortality in initially healthy men. J Gerontol A Biol Sci Med Sci 2000; 55A:M168-M173.
97. Dominguez LJ, Barbagallo M. The cardiometabolic syndrome and sarcopenic obesity in older persons. J Cardiometab Syndr 2007; 2:183-189. Changes in body composition and fat redistribution with aging are associated with obesity-related cardiometabolic risk factors. This article discusses the role of cardiometabolic syndrome in the development of sarcopenic obesity.
98. Aubertin-Leheudre M, Lord C, Goulet ED, et al. Effect of sarcopenia on cardiovascular disease risk factors in obese postmenopausal women. Obesity (Silver Spring) 2006; 14:2277-2283.
99. Hulens M, Vansant G, Claessens AL, et al. Predictors of 6-min walk test results in lean, obese and morbidly obese women. Scand J Med Sci Sports 2003; 13:98-105.
100. Hulens M, Vansant G, Lysens R, et al. Exercise capacity in lean versus obese women. Scand J Med Sci Sports 2001; 11:305-309.
101. Baumgartner RN, Wayne SJ, Waters DL, et al. Sarcopenic obesity predicts instrumental activities of daily living disability in the elderly. Obes Res 2004; 12:1995-2004.
102. Rantanen T, Volpato S, Ferrucci L, et al. Handgrip strength and cause-specific and total mortality in older disabled women: exploring the mechanism. J Am Geriatr Soc 2003; 51:636-641.
103. Gale CR, Martyn CN, Cooper C, Sayer AA. Grip strength, body composition, and mortality, Int J Epidemiol 2007; 36:228-235.
104. Zamboni M, Mazzali G, Zoico E, et al. Health consequences of obesity in the elderly: a review of four unresolved questions, Int J Obes (Lond) 2005; 29:1011-1029.
105. Al Snih S, Ottenbacher KJ, Markides KS, et al. The effect of obesity on disability vs mortality in older Americans. Arch Intern Med 2007; 167:774-780. A large 7-year follow-up study based on Established Populations for Epidemiologic Studies of the Elderly (EPESE) study confirming earlier findings that obesity is more important risk factor for disability than for mortality.
106. Flegal KM, Graubard BI, Williamson DF, Gail MH. Excess deaths associated with underweight, overweight, and obesity. JAMA 2005; 293:1861-1867.
107. Lafortuna CL, Maffiuletti NA, Agosti F, Sartorio A. Gender variations of body composition, muscle strength and power output in morbid obesity, Int J Obes 2005; 29:833-841.
108. Friedmann JM, Elasy T, Jensen GL. The relationship between body mass index and self-reported functional limitation among older adults: a gender difference. J Am Geriatr Soc 2001; 49:398-403.
109. Angleman SB, Harris TB, Melzer D. The role of waist circumference in predicting disability in periretirement age adults, Int J Obes 2006; 30:364-373.