Sarcopenia, frailty, and diabetes in older adults

Diabetes and Metabolism Journal

Volumn 40, Issue 3, 2016, Pages 182-189

  Jang, Hak Chul ^a  

^a Seoul National University Bundang Hospital   (South Korea)

Author keywords

Diabetes; Disability; Frailty; Sarcopenia

Indexed keywords

AEROBIC EXERCISE; ARTICLE; BODY MASS; CROSS-SECTIONAL STUDY; DIABETIC NEUROPATHY; DIET SUPPLEMENTATION; DIETARY REFERENCE INTAKE; DISEASE ASSOCIATION; ELECTROPHYSIOLOGY; FRAIL ELDERLY; GLYCEMIC CONTROL; HEALTH CARE COST; HUMAN; HYPERGLYCEMIA; INSULIN RESISTANCE; MUSCLE MASS; MUSCLE STRENGTH; NON INSULIN DEPENDENT DIABETES MELLITUS; OBESITY; PATHOPHYSIOLOGY; PROTEIN INTAKE; RESISTANCE TRAINING; RISK FACTOR; SARCOPENIA; WEIGHT REDUCTION;

EID: 84977136781     PISSN: 22336079     EISSN: 22336087     Source Type: Journal    
DOI: 10.4093/dmj.2016.40.3.182     Document Type: Article

References (69)

1. The Population Reference Bureau: 2014 World population data sheet. Available from: http://www.prb.org/pdf14/2014- world-population-data-sheet_eng.pdf (cited 2016 Feb 27).
2. Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F, Martin FC, Michel JP, Rolland Y, Schneider SM, Topinkova E, Vandewoude M, Zamboni M; European Working Group on Sarcopenia in Older People. Sarcopenia: European consensus on definition and diagnosis. Report of the European Working Group on Sarcopenia in Older People. Age Ageing 2010;39:412-23.
3. Abellan van Kan G. Epidemiology and consequences of sarcopenia. J Nutr Health Aging 2009;13:708-12.
4. Kim KM, Lim S, Choi KM, Kim JH, Yu SH, Kim TN, Song W, Lim JY, Won CW, Yoo HJ, Jang HC; Sarcopenia Study Group of Korean Geriatrics Society. Sarcopenia in Korea: prevalence and clinical aspects. J Korean Geriatr Soc 2015;19:1-8.
5. Fried LP, Guralnik JM. Disability in older adults: evidence regarding significance, etiology, and risk. J Am Geriatr Soc 1997;45:92-100.
6. Kim JH, Lim S, Choi SH, Kim KM, Yoon JW, Kim KW, Lim JY, Park KS, Jang HC. Sarcopenia: an independent predictor of mortality in community-dwelling older Korean men. J Gerontol A Biol Sci Med Sci 2014;69:1244-52.
7. Resnick HE, Harris MI, Brock DB, Harris TB. American Diabetes Association diabetes diagnostic criteria, advancing age, and cardiovascular disease risk profiles: results from the Third National Health and Nutrition Examination Survey. Diabetes Care 2000;23:176-80.
8. Kim DJ. The epidemiology of diabetes in Korea. Diabetes Metab J 2011;35:303-8.
9. Lee YJ, Jang HC, Kim EH, Kim HJ, Lee SB, Choi SH, Lim S, Park KU, Park YJ, Kim KW. Association between apolipoprotein E polymorphism and type 2 diabetes in subjects aged 65 or over. Korean Diabetes J 2008;32:30-7.
10. De Rekeneire N, Resnick HE, Schwartz AV, Shorr RI, Kuller LH, Simonsick EM, Vellas B, Harris TB; Health, Aging, and Body Composition study. Diabetes is associated with subclinical functional limitation in nondisabled older individuals: the Health, Aging, and Body Composition study. Diabetes Care 2003;26:3257-63.
11. Wong E, Backholer K, Gearon E, Harding J, Freak-Poli R, Stevenson C, Peeters A. Diabetes and risk of physical disability in adults: a systematic review and meta-analysis. Lancet Diabetes Endocrinol 2013;1:106-14.
12. Caruso LB, Silliman RA, Demissie S, Greenfield S, Wagner EH. What can we do to improve physical function in older persons with type 2 diabetes? J Gerontol A Biol Sci Med Sci 2000;55:M372-7.
13. Narayan KM, Boyle JP, Thompson TJ, Sorensen SW, Williamson DF. Lifetime risk for diabetes mellitus in the United States. JAMA 2003;290:1884-90.
14. 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.
15. Hughes VA, Frontera WR, Roubenoff R, Evans WJ, Singh MA. Longitudinal changes in body composition in older men and women: role of body weight change and physical activity. Am J Clin Nutr 2002;76:473-81.
16. 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.
17. Fielding RA, Vellas B, Evans WJ, Bhasin S, Morley JE, Newman AB, Abellan van Kan G, Andrieu S, Bauer J, Breuille D, Cederholm T, Chandler J, De Meynard C, Donini L, Harris T, Kannt A, Keime Guibert F, Onder G, Papanicolaou D, Rolland Y, Rooks D, Sieber C, Souhami E, Verlaan S, Zamboni M. Sarcopenia: an undiagnosed condition in older adults. Current consensus definition: prevalence, etiology, and consequences. International working group on sarcopenia. J Am Med Dir Assoc 2011;12:249-56.
18. Newman AB, Kupelian V, Visser M, Simonsick EM, Goodpaster BH, Kritchevsky SB, Tylavsky FA, Rubin SM, Harris TB. 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;61:72-7.
19. Landi F, Liperoti R, Russo A, Giovannini S, Tosato M, Capoluongo E, Bernabei R, Onder G. Sarcopenia as a risk factor for falls in elderly individuals: results from the ilSIRENTE study. Clin Nutr 2012;31:652-8.
20. Woo J, Leung J, Sham A, Kwok T. Defining sarcopenia in terms of risk of physical limitations: a 5-year follow-up study of 3,153 Chinese men and women. J Am Geriatr Soc 2009;57: 2224-31.
21. Studenski SA, Peters KW, Alley DE, Cawthon PM, McLean RR, Harris TB, Ferrucci L, Guralnik JM, Fragala MS, Kenny AM, Kiel DP, Kritchevsky SB, Shardell MD, Dam TT, Vassileva MT. The FNIH sarcopenia project: rationale, study description, conference recommendations, and final estimates. J Gerontol A Biol Sci Med Sci 2014;69:547-58.
22. Kim JH, Choi SH, Lim S, Yoon JW, Kang SM, Kim KW, Lim JY, Cho NH, Jang HC. Sarcopenia and obesity: gender-different relationship with functional limitation in older persons. J Korean Med Sci 2013;28:1041-7.
23. Kim KE, Jang SN, Lim S, Park YJ, Paik NJ, Kim KW, Jang HC, Lim JY. Relationship between muscle mass and physical performance: is it the same in older adults with weak muscle strength? Age Ageing 2012;41:799-803.
24. Lim S, Kim JH, Yoon JW, Kang SM, Choi SH, Park YJ, Kim KW, Lim JY, Park KS, Jang HC. Sarcopenic obesity: prevalence and association with metabolic syndrome in the Korean Longitudinal Study on Health and Aging (KLoSHA). Diabetes Care 2010;33:1652-4.
25. Kim KM, Lim S, Choi SH, Kim JH, Shin CS, Park KS, Jang HC. Cardiometabolic implication of sarcopenia: the Korea National Health and Nutrition Examination Study (KNHANES) 2008- 2010. IJC Metab Endocr 2014;4:63-9.
26. Park SW, Goodpaster BH, Strotmeyer ES, Kuller LH, Broudeau R, Kammerer C, de Rekeneire N, Harris TB, Schwartz AV, Tylavsky FA, Cho YW, Newman AB; Health, Aging, and Body Composition Study. Accelerated loss of skeletal muscle strength in older adults with type 2 diabetes: the health, aging, and body composition study. Diabetes Care 2007;30:1507-12.
27. Park SW, Goodpaster BH, Lee JS, Kuller LH, Boudreau R, de Rekeneire N, Harris TB, Kritchevsky S, Tylavsky FA, Nevitt M, Cho YW, Newman AB; Health, Aging, and Body Composition Study. Excessive loss of skeletal muscle mass in older adults with type 2 diabetes. Diabetes Care 2009;32:1993-7.
28. Sayer AA, Dennison EM, Syddall HE, Gilbody HJ, Phillips DI, Cooper C. Type 2 diabetes, muscle strength, and impaired physical function: the tip of the iceberg? Diabetes Care 2005; 28:2541-2.
29. Leenders M, Verdijk LB, van der Hoeven L, Adam JJ, van Kranenburg J, Nilwik R, van Loon LJ. Patients with type 2 diabetes show a greater decline in muscle mass, muscle strength, and functional capacity with aging. J Am Med Dir Assoc 2013; 14:585-92.
30. Volpato S, Bianchi L, Lauretani F, Lauretani F, Bandinelli S, Guralnik JM, Zuliani G, Ferrucci L. Role of muscle mass and muscle quality in the association between diabetes and gait speed. Diabetes Care 2012;35:1672-9.
31. Kalyani RR, Tra Y, Yeh HC, Egan JM, Ferrucci L, Brancati FL. Quadriceps strength, quadriceps power, and gait speed in older U.S. adults with diabetes mellitus: results from the National Health and Nutrition Examination Survey, 1999-2002. J Am Geriatr Soc 2013;61:769-75.
32. Kim KS, Park KS, Kim MJ, Kim SK, Cho YW, Park SW. Type 2 diabetes is associated with low muscle mass in older adults. Geriatr Gerontol Int 2014;14 Suppl 1:115-21.
33. Kim TN, Park MS, Yang SJ, Yoo HJ, Kang HJ, Song W, Seo JA, Kim SG, Kim NH, Baik SH, Choi DS, Choi KM. Prevalence and determinant factors of sarcopenia in patients with type 2 diabetes: the Korean Sarcopenic Obesity Study (KSOS). Diabetes Care 2010;33:1497-9.
34. Yoon JW, Ha YC, Kim KM, Moon JH, Choi SH, Lim S, Park YJ, Lim JY, Kim KW, Park KS, Jang HC. Hyperglycemia is associated with impaired muscle quality in older men with diabetes: the Korean Longitudinal Study on Health and Aging. Diabetes Metab J 2016;40:140-6.
35. Morley JE, Malmstrom TK, Rodriguez-Manas L, Sinclair AJ. Frailty, sarcopenia and diabetes. J Am Med Dir Assoc 2014; 15:853-9.
36. von Haehling S, Morley JE, Anker SD. From muscle wasting to sarcopenia and myopenia: update 2012. J Cachexia Sarcopenia Muscle 2012;3:213-7.
37. Wang X, Hu Z, Hu J, Du J, Mitch WE. Insulin resistance accelerates muscle protein degradation: activation of the ubiquitinproteasome pathway by defects in muscle cell signaling. Endocrinology 2006;147:4160-8.
38. Lawrence JC Jr. mTOR-dependent control of skeletal muscle protein synthesis. Int J Sport Nutr Exerc Metab 2001;11 Suppl: S177-85.
39. Dalal M, Ferrucci L, Sun K, Beck J, Fried LP, Semba RD. Elevated serum advanced glycation end products and poor grip strength in older community-dwelling women. J Gerontol A Biol Sci Med Sci 2009;64:132-7.
40. Semba RD, Bandinelli S, Sun K, Guralnik JM, Ferrucci L. Relationship of an advanced glycation end product, plasma carboxymethyl- lysine, with slow walking speed in older adults: the InCHIANTI study. Eur J Appl Physiol 2010;108:191-5.
41. Momma H, Niu K, Kobayashi Y, Guan L, Sato M, Guo H, Chujo M, Otomo A, Yufei C, Tadaura H, Saito T, Mori T, Miyata T, Nagatomi R. Skin advanced glycation end product accumulation and muscle strength among adult men. Eur J Appl Physiol 2011;111:1545-52.
42. Andreassen CS, Jakobsen J, Andersen H. Muscle weakness: a progressive late complication in diabetic distal symmetric polyneuropathy. Diabetes 2006;55:806-12.
43. Andersen H, Stalberg E, Gjerstad MD, Jakobsen J. Association of muscle strength and electrophysiological measures of reinnervation in diabetic neuropathy. Muscle Nerve 1998;21: 1647-54.
44. Partanen J, Niskanen L, Lehtinen J, Mervaala E, Siitonen O, Uusitupa M. Natural history of peripheral neuropathy in patients with non-insulin-dependent diabetes mellitus. N Engl J Med 1995;333:89-94.
45. Tuttle LJ, Sinacore DR, Cade WT, Mueller MJ. Lower physical activity is associated with higher intermuscular adipose tissue in people with type 2 diabetes and peripheral neuropathy. Phys Ther 2011;91:923-30.
46. Visser M, Pahor M, Taaffe DR, Goodpaster BH, Simonsick EM, Newman AB, Nevitt M, Harris TB. Relationship of interleukin- 6 and tumor necrosis factor-alpha with muscle mass and muscle strength in elderly men and women: the Health ABC Study. J Gerontol A Biol Sci Med Sci 2002;57:M326-32.
47. Cesari M, Penninx BW, Pahor M, Lauretani F, Corsi AM, Rhys Williams G, Guralnik JM, Ferrucci L. Inflammatory markers and physical performance in older persons: the InCHIANTI study. J Gerontol A Biol Sci Med Sci 2004;59:242-8.
48. Sinha-Hikim I, Cornford M, Gaytan H, Lee ML, Bhasin S. Effects of testosterone supplementation on skeletal muscle fiber hypertrophy and satellite cells in community-dwelling older men. J Clin Endocrinol Metab 2006;91:3024-33.
49. Fried LP, Tangen CM, Walston J, Newman AB, Hirsch C, Gottdiener J, Seeman T, Tracy R, Kop WJ, Burke G, McBurnie MA; Cardiovascular Health Study Collaborative Research Group. Frailty in older adults: evidence for a phenotype. J Gerontol A Biol Sci Med Sci 2001;56:M146-56.
50. Rodriguez-Manas L, Feart C, Mann G, Vina J, Chatterji S, Chodzko-Zajko W, Gonzalez-Colaco Harmand M, Bergman H, Carcaillon L, Nicholson C, Scuteri A, Sinclair A, Pelaez M, Van der Cammen T, Beland F, Bickenbach J, Delamarche P, Ferrucci L, Fried LP, Gutierrez-Robledo LM, Rockwood K, Rodriguez Artalejo F, Serviddio G, Vega E; FOD-CC group (Appendix 1). Searching for an operational definition of frailty: a Delphi method based consensus statement: the frailty operative definition-consensus conference project. J Gerontol A Biol Sci Med Sci 2013;68:62-7.
51. Fried LP, Walston J. Principles of geriatric medicine and gerontology. 5th ed. New York: McGraw Hill; 2003. Chapter 116, Frailty and failure to thrive; p1487-502.
52. Ottenbacher KJ, Graham JE, Al Snih S, Raji M, Samper-Ternent R, Ostir GV, Markides KS. Mexican Americans and frailty: findings from the Hispanic established populations epidemiologic studies of the elderly. Am J Public Health 2009;99:673-9.
53. Hubbard RE, Andrew MK, Fallah N, Rockwood K. Compari son of the prognostic importance of diagnosed diabetes, comorbidity and frailty in older people. Diabet Med 2010;27:603- 6.
54. Cacciatore F, Testa G, Galizia G, Della-Morte D, Mazzella F, Langellotto A, Pirozzi G, Ferro G, Gargiulo G, Ferrara N, Rengo F, Abete P. Clinical frailty and long-term mortality in elderly subjects with diabetes. Acta Diabetol 2013;50:251-60.
55. Saum KU, Dieffenbach AK, Muller H, Holleczek B, Hauer K, Brenner H. Frailty prevalence and 10-year survival in community- dwelling older adults: results from the ESTHER cohort study. Eur J Epidemiol 2014;29:171-9.
56. Bouillon K, Kivimaki M, Hamer M, Shipley MJ, Akbaraly TN, Tabak A, Singh-Manoux A, Batty GD. Diabetes risk factors, diabetes risk algorithms, and the prediction of future frailty: the Whitehall II prospective cohort study. J Am Med Dir Assoc 2013;14:851.e1-6.
57. Rolland Y, Onder G, Morley JE, Gillette-Guyonet S, Abellan van Kan G, Vellas B. Current and future pharmacologic treatment of sarcopenia. Clin Geriatr Med 2011;27:423-47.
58. Frankel JE, Bean JF, Frontera WR. Exercise in the elderly: research and clinical practice. Clin Geriatr Med 2006;22:239-56; vii.
59. Short KR, Vittone JL, Bigelow ML, Proctor DN, Nair KS. Age and aerobic exercise training effects on whole body and muscle protein metabolism. Am J Physiol Endocrinol Metab 2004;286:E92-101.
60. Misic MM, Rosengren KS, Woods JA, Evans EM. Muscle quality, aerobic fitness and fat mass predict lower-extremity physical function in community-dwelling older adults. Gerontology 2007;53:260-6.
61. Sipila S, Suominen H. Effects of strength and endurance training on thigh and leg muscle mass and composition in elderly women. J Appl Physiol (1985) 1995;78:334-40.
62. Frontera WR, Meredith CN, O'Reilly KP, Knuttgen HG, Evans WJ. Strength conditioning in older men: skeletal muscle hypertrophy and improved function. J Appl Physiol (1985) 1988; 64:1038-44.
63. Taaffe DR, Duret C, Wheeler S, Marcus R. Once-weekly resistance exercise improves muscle strength and neuromuscular performance in older adults. J Am Geriatr Soc 1999;47:1208- 14.
64. Bartali B, Frongillo EA, Bandinelli S, Lauretani F, Semba RD, Fried LP, Ferrucci L. Low nutrient intake is an essential component of frailty in older persons. J Gerontol A Biol Sci Med Sci 2006;61:589-93.
65. Houston DK, Nicklas BJ, Ding J, Harris TB, Tylavsky FA, Newman AB, Lee JS, Sahyoun NR, Visser M, Kritchevsky SB; Health ABC Study. 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;87:150-5.
66. Castaneda C, Charnley JM, Evans WJ, Crim MC. Elderly women accommodate to a low-protein diet with losses of body cell mass, muscle function, and immune response. Am J Clin Nutr 1995;62:30-9.
67. Campbell WW, Trappe TA, Wolfe RR, Evans WJ. The recommended dietary allowance for protein may not be adequate for older people to maintain skeletal muscle. J Gerontol A Biol Sci Med Sci 2001;56:M373-80.
68. Bonnefoy M, Cornu C, Normand S, Boutitie F, Bugnard F, Rahmani A, Lacour JR, Laville M. The effects of exercise and protein-energy supplements on body composition and muscle function in frail elderly individuals: a long-term controlled randomised study. Br J Nutr 2003;89:731-9.
69. Milne AC, Potter J, Vivanti A, Avenell A. Protein and energy supplementation in elderly people at risk from malnutrition. Cochrane Database Syst Rev 2009;(2):CD003288.