Journal List > J Korean Diabetes > v.18(4) > 1055073

Kim and Yu: Diabetes and Sarcopenia

Abstract

Sarcopenia is defined as the loss of muscle mass and strength that occurs with aging. Although the etiology, pathogenesis, and diagnosis of sarcopenia are obscure, sarcopenia has been suggested to play a pivotal role in the pathogenesis of frailty and functional impairment in diabetes. The aim of this article was to provide an overview of the pathogenesis, diagnosis, epidemiology, and clinical implications of sarcopenia and the relationship between diabetes and sarcopenia.

References

1. Statistics Korea. Available from:. http://kosis.kr/statHtml/statHtml.do?orgId=101&tblId=DT_1BPA003&conn_path=I2. (updated 2017 Jan 26).
2. Whiting DR, Guariguata L, Weil C, Shaw J. IDF diabetes atlas: global estimates of the prevalence of diabetes for 2011 and 2030. Diabetes Res Clin Pract. 2011; 94:311–21.
crossref
3. 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 metaanalysis. Lancet Diabetes Endocrinol. 2013; 1:106–14.
crossref
4. 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. International Working Group on Sarcopenia. Sarcopenia: an undiagnosed condition in older adults. Current consensus definition: prevalence, etiology, and consequences. J Am Med Dir Assoc. 2011; 12:249–56.
5. Rosenberg IH. Summary comments. Am J Clin Nutr. 1989; 50:1231–3.
crossref
6. 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.
crossref
7. 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.
crossref
8. Delmonico MJ, Harris TB, Lee JS, Visser M, Nevitt M, Kritchevsky SB, Tylavsky FA, Newman AB. Health, Aging and Body Composition Study. Alternative definitions of sarcopenia, lower extremity performance, and functional impairment with aging in older men and women. J Am Geriatr Soc. 2007; 55:769–74.
crossref
9. Carey KA, Farnfield MM, Tarquinio SD, Cameron-Smith D. Impaired expression of Notch signaling genes in aged human skeletal muscle. J Gerontol A Biol Sci Med Sci. 2007; 62:9–17.
crossref
10. Welle S, Brooks AI, Delehanty JM, Needler N, Thornton CA. Gene expression profile of aging in human muscle. Physiol Genomics. 2003; 14:149–59.
crossref
11. Campbell WW, Crim MC, Dallal GE, Young VR, Evans WJ. Increased protein requirements in elderly people: new data and retrospective reassessments. Am J Clin Nutr. 1994; 60:501–9.
crossref
12. Katsanos CS, Kobayashi H, Sheffield-Moore M, Aarsland A, Wolfe RR. Aging is associated with diminished accretion of muscle proteins after the ingestion of a small bolus of essential amino acids. Am J Clin Nutr. 2005; 82:1065–73.
crossref
13. Visser M, Deeg DJ, Lips P. Longitudinal Aging Study Amsterdam. Low vitamin D and high parathyroid hormone levels as determinants of loss of muscle strength and muscle mass (sarcopenia): the Longitudinal Aging Study Amsterdam. J Clin Endocrinol Metab. 2003; 88:5766–72.
crossref
14. Volpi E, Sheffield-Moore M, Rasmussen BB, Wolfe RR. Basal muscle amino acid kinetics and protein synthesis in healthy young and older men. JAMA. 2001; 286:1206–12.
crossref
15. Baumgartner RN, Waters DL, Gallagher D, Morley JE, Garry PJ. Predictors of skeletal muscle mass in elderly men and women. Mech Ageing Dev. 1999; 107:123–36.
crossref
16. Guillet C, Boirie Y. Insulin resistance: a contributing factor to age-related muscle mass loss? Diabetes Metab. 2005; 31:5S20–5S26.
crossref
17. Morley JE. Hormones and the aging process. J Am Geriatr Soc. 2003; 51(7 Suppl):S333–7.
crossref
18. 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.
19. McDermott MM, Guralnik JM, Albay M, Bandinelli S, Miniati B, Ferrucci L. Impairments of muscles and nerves associated with peripheral arterial disease and their relationship with lower extremity functioning: the InCHIANTI Study. J Am Geriatr Soc. 2004; 52:405–10.
crossref
20. Ferrucci L, Penninx BW, Volpato S, Harris TB, Bandeen-Roche K, Balfour J, Leveille SG, Fried LP, Md JM. Change in muscle strength explains accelerated decline of physical function in older women with high interleukin-6 serum levels. J Am Geriatr Soc. 2002; 50:1947–54.
crossref
21. 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.
crossref
22. 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.
crossref
23. Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F, Martin FC, Michel JP, Rolland Y, Schneider SM, Topinková 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.
crossref
24. Kim J, Wang Z, Heymsfield SB, Baumgartner RN, Gallagher D. Total-body skeletal muscle mass: estimation by a new dual-energy X-ray absorptiometry method. Am J Clin Nutr. 2002; 76:378–83.
crossref
25. NIH Consensus statement. Bioelectrical impedance analysis in body composition measurement. National Institutes of Health Technology Assessment Conference Statement. December 12–14, 1994. Nutrition. 1996; 12:749–62.
26. Janssen I, Heymsfield SB, Baumgartner RN, Ross R. Estimation of skeletal muscle mass by bioelectrical impedance analysis. J Appl Physiol (1985). 2000; 89:465–71.
crossref
27. Lauretani F, Russo CR, Bandinelli S, Bartali B, Cavazzini C, Di Iorio A, Corsi AM, Rantanen T, Guralnik JM, Ferrucci L. Age-associated changes in skeletal muscles and their effect on mobility: an operational diagnosis of sarcopenia. J Appl Physiol (1985). 2003; 95:1851–60.
crossref
28. Pahor M, Manini T, Cesari M. Sarcopenia: clinical evaluation, biological markers and other evaluation tools. J Nutr Health Aging. 2009; 13:724–8.
crossref
29. Park SW, Goodpaster BH, Strotmeyer ES, de Rekeneire N, Harris TB, Schwartz AV, Tylavsky FA, Newman AB. Decreased muscle strength and quality in older adults with type 2 diabetes: the health, aging, and body composition study. Diabetes. 2006; 55:1813–8.
30. 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.
crossref
31. 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.
crossref
32. Amati F, Dubé JJ, Coen PM, Stefanovic-Racic M, Toledo FG, Goodpaster BH. Physical inactivity and obesity underlie the insulin resistance of aging. Diabetes Care. 2009; 32:1547–9.
crossref
33. Karakelides H, Nair KS. Sarcopenia of aging and its metabolic impact. Curr Top Dev Biol. 2005; 68:123–48.
crossref
34. Cleasby ME, Jamieson PM, Atherton PJ. Insulin resistance and sarcopenia: mechanistic links between common comorbidities. J Endocrinol. 2016; 229:R67–81.
crossref
35. Lang CH, Frost RA, Nairn AC, MacLean DA, Vary TC. TNF-alpha impairs heart and skeletal muscle protein synthesis by altering translation initiation. Am J Physiol Endocrinol Metab. 2002; 282:E336–47.
36. Srikanthan P, Hevener AL, Karlamangla AS. Sarcopenia exacerbates obesity-associated insulin resistance and dysglycemia: findings from the National Health and Nutrition Examination Survey III. PLoS One. 2010; 5:e10805.
crossref
37. Srikanthan P, Karlamangla AS. Relative muscle mass is inversely associated with insulin resistance and prediabetes. Findings from the third National Health and Nutrition Examination Survey. J Clin Endocrinol Metab. 2011; 96:2898–903.
crossref
38. Moon SS. Low skeletal muscle mass is associated with insulin resistance, diabetes, and metabolic syndrome in the Korean population: the Korea National Health and Nutrition Examination Survey (KNHANES) 2009–2010. Endocr J. 2014; 61:61–70.
crossref
39. Kim TN, Park MS, Lim KI, Choi HY, Yang SJ, Yoo HJ, Kang HJ, Song W, Choi H, Baik SH, Choi DS, Choi KM. Relationships between sarcopenic obesity and insulin resistance, inflammation, and vitamin D status: the Korean Sarcopenic Obesity Study. Clin Endocrinol (Oxf). 2013; 78:525–32.
crossref
40. Cadore EL, Izquierdo M. New strategies for the concurrent strength-, power-, and endurance-training prescription in elderly individuals. J Am Med Dir Assoc. 2013; 14:623–4.
crossref
41. Singh NA, Quine S, Clemson LM, Williams EJ, Williamson DA, Stavrinos TM, Grady JN, Perry TJ, Lloyd BD, Smith EU, Singh MA. Effects of high-intensity progressive resistance training and targeted multidisciplinary treatment of frailty on mortality and nursing home admissions after hip fracture: a randomized controlled trial. J Am Med Dir Assoc. 2012; 13:24–30.
crossref
42. Valenzuela T. Efficacy of progressive resistance training interventions in older adults in nursing homes: a systematic review. J Am Med Dir Assoc. 2012; 13:418–28.
crossref
43. Pahor M, Guralnik JM, Ambrosius WT, Blair S, Bonds DE, Church TS, Espeland MA, Fielding RA, Gill TM, Groessl EJ, King AC, Kritchevsky SB, Manini TM, McDermott MM, Miller ME, Newman AB, Rejeski WJ, Sink KM, Williamson JD. LIFE study investigators. Effect of structured physical activity on prevention of major mobility disability in older adults: the LIFE study randomized clinical trial. JAMA. 2014; 311:2387–96.
44. Bauer J, Biolo G, Cederholm T, Cesari M, Cruz-Jentoft AJ, Morley JE, Phillips S, Sieber C, Stehle P, Teta D, Visvanathan R, Volpi E, Boirie Y. Evidence-based recommendations for optimal dietary protein intake in older people: a position paper from the PROT-AGE Study Group. J Am Med Dir Assoc. 2013; 14:542–59.
crossref
45. Bauer JM, Verlaan S, Bautmans I, Brandt K, Donini LM, Maggio M, McMurdo ME, Mets T, Seal C, Wijers SL, Ceda GP, De Vito G, Donders G, Drey M, Greig C, Holmbäck U, Narici M, McPhee J15, Poggiogalle E, Power D, Scafoglieri A, Schultz R, Sieber CC, Cederholm T. Effects of a vitamin D and leucine-enriched whey protein nutritional supplement on measures of sarcopenia in older adults, the PROVIDE study: a randomized, double-blind, placebo-controlled trial. J Am Med Dir Assoc. 2015; 16:740–7.
crossref
46. Morley JE, Argiles JM, Evans WJ, Bhasin S, Cella D, Deutz NE, Doehner W, Fearon KC, Ferrucci L, Hellerstein MK, Kalantar-Zadeh K, Lochs H, MacDonald N, Mulligan K, Muscaritoli M, Ponikowski P, Posthauer ME, Rossi Fanelli F, Schambelan M, Schols AM, Schuster MW, Anker SD. Society for Sarcopenia, Cachexia, and Wasting Disease. Nutritional recommendations for the management of sarcopenia. J Am Med Dir Assoc. 2010; 11:391–6.
crossref
47. Volpi E, Campbell WW, Dwyer JT, Johnson MA, Jensen GL, Morley JE, Wolfe RR. Is the optimal level of protein intake for older adults greater than the recommended dietary allowance? J Gerontol A Biol Sci Med Sci. 2013; 68:677–81.
crossref
48. Beaudart C, Buckinx F, Rabenda V, Gillain S, Cavalier E, Slomian J, Petermans J, Reginster JY, Bruyère O. The effects of vitamin D on skeletal muscle strength, muscle mass, and muscle power: a systematic review and metaanalysis of randomized controlled trials. J Clin Endocrinol Metab. 2014; 99:4336–45.
crossref
49. Muir SW, Montero-Odasso M. Effect of vitamin D supplementation on muscle strength, gait and balance in older adults: a systematic review and metaanalysis. J Am Geriatr Soc. 2011; 59:2291–300.
crossref
50. Srinivas-Shankar U, Roberts SA, Connolly MJ, O'Connell MD, Adams JE, Oldham JA, Wu FC. Effects of testosterone on muscle strength, physical function, body composition, and quality of life in intermediate-frail and frail elderly men: a randomized, double-blind, placebo-controlled study. J Clin Endocrinol Metab. 2010; 95:639–50.
crossref
51. Travison TG, Basaria S, Storer TW, Jette AM, Miciek R, Farwell WR, Choong K, Lakshman K, Mazer NA, Coviello AD, Knapp PE, Ulloor J, Zhang A, Brooks B, Nguyen AH, Eder R, LeBrasseur N, Elmi A, Appleman E, Hede-Brierley L, Bhasin G, Bhatia A, Lazzari A, Davis S, Ni P, Collins L, Bhasin S. Clinical meaningfulness of the changes in muscle performance and physical function associated with testosterone administration in older men with mobility limitation. J Gerontol A Biol Sci Med Sci. 2011; 66:1090–9.
crossref
52. Snyder PJ, Bhasin S, Cunningham GR, Matsumoto AM, Stephens-Shields AJ, Cauley JA, Gill TM, Barrett-Connor E, Swerdloff RS, Wang C, Ensrud KE, Lewis CE, Farrar JT, Cella D, Rosen RC, Pahor M, Crandall JP, Molitch ME, Cifelli D, Dougar D, Fluharty L, Resnick SM, Storer TW, Anton S, Basaria S, Diem SJ, Hou X, Mohler ER 3rd, Parsons JK, Wenger NK, Zeldow B, Landis JR, Ellenberg SS. Testosterone Trials Investigators. Effects of testosterone treatment in older men. N Engl J Med. 2016; 374:611–24.
crossref
53. Morley JE, von Haehling S, Anker SD. Are we closer to having drugs to treat muscle wasting disease? J Cachexia Sarcopenia Muscle. 2014; 5:83–7.
crossref
54. Dalton JT, Barnette KG, Bohl CE, Hancock ML, Rodriguez D, Dodson ST, Morton RA, Steiner MS. The selective androgen receptor modulator GTx-024 (enobosarm) improves lean body mass and physical function in healthy elderly men and postmenopausal women: results of a double-blind, placebo-controlled phase II trial. J Cachexia Sarcopenia Muscle. 2011; 2:153–61.
crossref
55. Ebner N, Steinbeck L, Doehner W, Anker SD, von Haehling S. Highlights from the 7th Cachexia Conference: muscle wasting pathophysiological detection and novel treatment strategies. J Cachexia Sarcopenia Muscle. 2014; 5:27–34.
crossref
56. Kalyani RR, Tian J, Xue QL, Walston J, Cappola AR, Fried LP, Brancati FL, Blaum CS. Hyperglycemia and incidence of frailty and lower extremity mobility limitations in older women. J Am Geriatr Soc. 2012; 60:1701–7.
crossref
57. Wang CP, Hazuda HP. Better glycemic control is associated with maintenance of lower-extremity function over time in Mexican American and European American older adults with diabetes. Diabetes Care. 2011; 34:268–73.
crossref
58. 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.
crossref
59. Abdelhafiz AH, Rodríguez-Mañas L, Morley JE, Sinclair AJ. Hypoglycemia in older people-a less well recognized risk factor for frailty. Aging Dis. 2015; 6:156–67.
60. Yau CK, Eng C, Cenzer IS, Boscardin WJ, Rice-Trumble K, Lee SJ. Glycosylated hemoglobin and functional decline in community-dwelling nursing home-eligible elderly adults with diabetes mellitus. J Am Geriatr Soc. 2012; 60:1215–21.
crossref

Table 1.
European Working Group on Sarcopenia in Older People (EWGSOP) criteria for sarcopenia
Stage Muscle mass Muscle strength   Performance
Presarcopenia      
Sarcopenia Or
Severe sarcopenia  

Adapted from the article of Cruz-Jentoft et al. Age Ageing (2010;39:412–23) [23].

TOOLS
Similar articles