Skip Navigation
Skip to contents

Diabetes Metab J : Diabetes & Metabolism Journal

Search
OPEN ACCESS

Articles

Page Path
HOME > Diabetes Metab J > Volume 40(3); 2016 > Article
Sulwon Lecture 2015
Clinical Care/Education Sarcopenia, Frailty, and Diabetes in Older Adults
Hak Chul Jangorcid
Diabetes & Metabolism Journal 2016;40(3):182-189.
DOI: https://doi.org/10.4093/dmj.2016.40.3.182
Published online: April 20, 2016
  • 6,660 Views
  • 144 Download
  • 80 Web of Science
  • 77 Crossref
  • 89 Scopus

Department of Internal Medicine, Seoul National University Bundang Hospital, Seoul National University College of Medicine, Seongnam, Korea.

Corresponding author: Hak Chul Jang. Department of Internal Medicine, Seoul National University Bundang Hospital, Seoul National University College of Medicine, 82 Gumi-ro 173beon-gil, Bundang-gu, Seongnam 13620, Korea. janghak@snu.ac.kr
• Received: February 10, 2016   • Accepted: March 5, 2016

Copyright © 2016 Korean Diabetes Association

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

  • Populations are aging and the prevalence of diabetes mellitus is increasing tremendously. The number of older people with diabetes is increasing unexpectedly. Aging and diabetes are both risk factors for functional disability. Thus, increasing numbers of frail or disabled older patients with diabetes will increase both direct and indirect health-related costs. Diabetes has been reported as an important risk factor of developing physical disability in older adults. Older people with diabetes have lower muscle mass and weaker muscle strength. In addition, muscle quality is poorer in diabetic patients. Sarcopenia and frailty have a common soil and may share a similar pathway for multiple pathologic processes in older people. Sarcopenia is thought to be an intermediate step in the development of frailty in patients with diabetes. Thus, early detection of sarcopenia and frailty in older adults with diabetes should be routine clinical practice to prevent frailty or to intervene earlier in frail patients.
The Sulwon Award for Scientific Achievement is the Korean Diabetes Association's highest scientific award and honors an individual who has excellently contributed to the progress in the field of diabetes and metabolism. Sulwon Award is named after an emeritus professor Eung Jin Kim, who founded Korean Diabetes Association. Prof. Hak Chul Jang received the seventh Sulwon Award at 2015 International Conference on Diabetes and Metabolism, October 15-17, 2015 at Jejudo Island, Korea.
Increased life expectancy and declining fertility has brought dramatic shifts in the age structure worldwide [1]. Large populations are aging and this has become a global social and health burden. A progressive decline in muscle mass and strength, termed sarcopenia, develops as a consequence of aging [2]. The prevalence of sarcopenia reported varies widely depending on the definition and methods of assessment; it ranges from 8% to 40% of people aged over 60 years [34]. Sarcopenia results in frailty, loss of independence, physical disability, and increased mortality in older adults [56].
Diabetes mellitus is a prevalent chronic disease, especially in older adults, that is associated with microvascular and cardiovascular complications [7]. More than 25% of Korean people over age 60 years have diabetes mellitus [89]. Diabetes has been associated with an increased risk of developing physical disability in older adults [1011]. Chronic conditions such as visual disturbances, diabetic complications, comorbidities, and depression are associated with physical disability in patients with diabetes; however, these account for only some of the impairments [12]. It was also reported that men and women with diabetes diagnosed at age 60 have estimated reductions in life expectancy of 7.3 and 9.5 years and good quality of life of 11.1 and 13.8 years, respectively [13]
Physical and cognitive function becomes of great importance in the care of older people with diabetes. A key strategy is to prevent the functional decline instead of attempting to recover lost function. In this review, the relationship between sarcopenia, frailty, and physical disability in older adults with diabetes will be discussed.
A progressive decrease in muscle mass, especially of the lower extremities and an increase in fat mass, especially of visceral and intermuscular fat are common body compositional changes associated with aging [1415]. After 30 years of age, muscle mass is reported to decline at an annual rate of approximately 1% to 2%, and that accelerates to as much as 1.5% to 3% per year after age 60 years, becoming ever faster after age 75 years (Fig. 1) [415].
Baumgartner et al. [16] first proposed that the appendicular skeletal muscle mass (ASM) divided by height squared (ASM/ht2) was as a representative muscle index. Clinically, sarcopenia was defined as relative ASM index less than 2 standard deviations below the mean values of healthy young adults or the lowest quintile of study populations [1617]. However, recent studies have indicated that decline in muscle strength may be more important in the health outcomes related to sarcopenia [18]. Based on this, the European Working Group for Sarcopenia in Older People proposed reduced muscle mass with either muscle weakness or poor physical performance as the criteria for sarcopenia [2]. These criteria demonstrated better associations with various outcomes compared with the definitions driven only by muscle mass [1920].
Meanwhile, the Foundation for the National Institutes of Health (FNIH) Sarcopenia Project has suggested a new criteria for sarcopenia categorized by muscle mass, muscle strength, and physical performance [21]. They proposed a new muscle mass index of ASM divided by body mass index. However, data about the clinical implications of the new FNIH criteria remain sparse.
Muscles play various important roles in the human body; thus, loss of muscle mass and strength can cause a diverse range of functional disability and metabolic derangements in older adults. Sarcopenia has been closely related to many clinical consequences, including functional disability, metabolic impairment, increased cardiovascular risk, and mortality, in the older Korean adults [622232425].
However, studies of sarcopenia in older adults with diabetes are few. The Health, Aging, and Body Composition (Health ABC) Study showed that older adults with type 2 diabetes lost their knee extensor strength more rapidly than nondiabetic subjects did [26]. In that study, diabetic patients had greater declines in muscle mass and leg muscle strength, and muscle quality was poorer in diabetic patients over 3 years. In addition, thigh muscle cross-sectional area also declined twice as fast in older women with diabetes than in nondiabetic subjects over 6 years [27]. Further, the Hertfordshire study demonstrated that older men newly diagnosed with diabetes have significantly weaker muscle strength and higher odds of impaired physical function than those without diabetes do [28]. Leenders et al. [29] also showed that leg lean mass and appendicular skeletal mass were significantly lower in older men with diabetes. Further, leg-extension strength in patients with diabetes was weaker than in nondiabetic subjects, and functional performance was impaired in older diabetic men. Other studies also have demonstrated that leg muscle strength and gait speed is reduced in older peoples with diabetes [3031]
Kim et al. [32] reported that in Korean men and women aged ≥65 years, ASM was lower in diabetic patients compared with nondiabetic subjects but relative muscle index (ASM/height2) was lower only in older men with diabetes. The Korean Sarcopenic Obesity Study showed that sarcopenia (skeletal muscle mass/weight×100 <2 SD below the mean of the young reference) was present in 15.7% in subjects with diabetes and 6.9% in the control subjects [33]. Yoon et al. [34] demonstrated that muscle mass and strength in older diabetic patients were not different compared with nondiabetic subjects, but muscle quality was poorer and physical performance was impaired in diabetic subjects with poor glycemic control.
Multiple factors are associated with decreased muscle mass and/or strength in older adults. [217] The major causes or mechanisms related to sarcopenia include inadequate nutrition, physical inactivity or disuse, age-related hormonal changes including sex hormone and growth hormone, loss of motor neurons, atherosclerosis, obesity, insulin resistance, and inflammatory cytokines (Table 1).
Additionally, diabetes mellitus will accelerate the reduction of muscle mass and strength because hyperglycemia, diabetic complications, obesity, insulin resistance, inflammatory cytokines, and endocrine changes associated with diabetes have adverse effects on muscle [35].
The mechanism of hyperglycemia that is associated with accelerated reduction of muscle mass and strength is still unclear. Weight loss associated with hyperglycemia may result in the loss of muscle mass and strength [36]. It is also reported that amino acid metabolism decreases in type 2 diabetes [37]. Insulin resistance inhibits the mammalian target of the rapamycin pathway that leads to protein synthesis and decreases protein degradation [38]. Insulin resistance also increases activation of the ubiquitin-proteasome pathway, resulting in degradation of muscle protein [37].
Chronic hyperglycemia increases advanced glycation end products (AGEs). AGEs accumulate in skeletal muscle and cartilage and increase the stiffness in patients with diabetes. It was reported that elevated AGEs were associated with poor grip strength in older women with moderate to severe disability and slow walking speed in older community-dwelling adults [39,40]. Higher skin autofluorescence, a noninvasive measurement of tissue AGEs, has been associated with lower grip strength and leg-extension power in Japanese men [41].
Another major cause of sarcopenia in diabetes is a decrease in motor neurons [42]. Diabetic neuropathy is a common complication of diabetes, especially in older adults, and it leads to muscle wasting and weakness of distal skeletal muscles [31]. Electrophysiological studies have shown that muscle strength of the ankle and knee extensors in patients with diabetes are correlated with fiber density and the amplitude of the macro motor unit potential [43], suggesting the loss of muscle strength because of incomplete reinnervation after axonal loss. A longitudinal follow-up study for diabetic polyneuropathy has shown that 8.3% of the patients had electrophysiological abnormalities at baseline; 16.7% had such abnormalities at 5 years; and 41.9% at 10 years [44]. Interestingly, diabetic patients with peripheral neuropathy had higher calf intermuscular adipose tissue volume, and higher adipose tissue volume was associated with poor muscle strength and physical function [45].
Diabetes is associated with an increase in inflammatory cytokines. It has been reported that systemic inflammatory cytokines such as tumor necrosis factor and interleukin 6 have detrimental effects on muscle mass, strength, and physical performance in older adults [4647].
Testosterone increases satellite cell numbers and protein synthesis in muscle [48]. Serum testosterone levels decline gradually and progressively with aging in men. The men with diabetes and/or obesity have lower serum testosterone levels. Therefore, testosterone deficiency is another cause of sarcopenia in patients with diabetes.
Frailty is a common geriatric syndrome in older adults that carries an increased risk for poor health outcomes including falls, incident disability, hospitalization, and mortality because of decreased physical reserves [49]. Although agreement between a theoretical concept and an operational definition is lacking [50], Fried et al. [49] defined a clinical phenotype of frailty, which was identified by the presence of three or more of the five components (Table 2). An individual with one or two of the five components was considered prefrail. Frailty seems to be a dynamic process and also potentially reversible. Therefore, early detection of frailty and prevention or early interventions should be key issues in the care of older adults.
Fried et al. [51] also proposed the cycle of frailty, in which sarcopenia was one of the main potential causes of frailty. Actually, sarcopenia and frailty have a commonality and may share the similar pathway for multiple pathologic processes in older people. Thus, sarcopenia may be an intermediate step in the development of frailty in patients with diabetes.
Several studies have shown that diabetic patients aged 65 years or older were more likely to be frail than nondiabetic older adults were [525354]. These studies also reported that frail patients with diabetes had a higher mortality than nonfrail patients, and the presence of frailty was an independent risk factor for mortality. The German ESTHER (Epidemiologische Studie zu Chancen der Verhütung, Früherkennung und optimierten Therapie chronischer Erkrankungen in der älteren Bevölkerung) study and the Whitehall II Prospective Study demonstrated that the prevalence of frailty was 3- to 5-fold higher in patients with diabetes older than 65 years than that seen in the general population [5556].
Morley et al. [35] suggested that the management of frailty in patients with diabetes initially should focus on the prevention of sarcopenia. Several consensus reports recommended the measurement of gait speed as a screening method on clinical practice [217]. Until now, no pharmacologic agent to prevent or treat sarcopenia has proven to be as efficacious as exercise (mainly resistance training) is in combination with nutritional intervention (adequate protein and energy intake) [57]. This approach is currently the key strategy for the management of sarcopenia and frailty.
Larger muscles in the body move in a rhythmic manner for a prolonged period during aerobic exercise, whereas resistance exercise involves muscles working hard against an applied force or weight such as in weight lifting. Both aerobic and resistance exercise training have been shown to prevent the decline in muscle mass and strength with age [58]. Although aerobic exercise is less likely to contribute to muscle hypertrophy, it has been linked to improvements in cardiovascular fitness and endurance capacity. Aerobic exercise can also reduce body fat including intra- and intermuscular fat, which in turn improves the functional role of muscle relative to body weight [5960]. In contrast, resistance exercise training appears to have a larger effect on augmenting muscle mass and strength, and it attenuates the development of sarcopenia [6162]. Improvements in muscle strength can be achieved with as little as one resistance exercise training session per week [63].
Many older people do not consume sufficient amounts of dietary intake and protein, which leads to a reduction in lean body mass and increased functional disability [64]. The current recommended dietary allowance (RDA) of dietary protein is 0.8 g/kg/day, but 40% of people aged over 70 years did not meet this RDA [65]. Older women taking a low protein diet below the RDA had a significant decline in muscle mass and strength [66]. Further, older people who took the protein of RDA had a negative nitrogen balance and might require a higher protein content than the RDA to maintain their skeletal muscle [67]. Although older adults who exercise may have additional protein requirements, studies investigating whether nutritional supplementation in combination with resistance exercise can augment muscle strength and mass have yielded inconsistent results [68]. Nutritional supplementation may result in an overall decrease in voluntary food intake and adherence to the supplements can be a problem [69].
Additionally, three treatable causes should be managed for the treatment of frailty [35]: (1) treatable causes of fatigue: vitamin B12 deficiency, adrenal inefficiency, hypothyroidism, anemia, sleep apnea, hypotension, syncope, and depression; (2) polypharmacy: anticholinergic medication, overtreatment of blood pressure, hypoglycemia; (3) and unintentional weight loss: depression, medications, dysphagia, dental problems, and nosocomial infections.
As larger populations are now aging, there is a tremendous increase of older adults with diabetes. Aging and diabetes are both risk factors for functional impairment. A recent systematic review article showed that diabetes is associated with a strong increase in the risk of physical disability in older adults [11]. This will increase both direct and indirect health-related costs. I believe that early detection of sarcopenia and frailty in older adults with diabetes should be routine clinical practice to facilitate early multimodal interventions.
Acknowledgements
This work was supported by the National Research Foundation Grant (No. 2006-2005410) of the Ministry of Education, Science, and Technology and a grant of the Korea Health Technology R&D Project through the Korea Health Industry Development Institute (KHIDI), funded by the Ministry of Health and Welfare, Republic of Korea (grant number: HI15C3207). I thank Professors Hyung-Joon Yoo and Ki-Up Lee for the scientific leadership in the field of elderly diabetes.

CONFLICTS OF INTEREST: No potential conflict of interest relevant to this article was reported.

  • 1. The Population Reference Bureau: 2014 World population data sheet cited 2016 Feb 27. Available from: http://www.prb.org/pdf14/2014-world-population-data-sheet_eng.pdf.
  • 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;39:412-423. PubMedPMC
  • 3. Abellan van Kan G. Epidemiology and consequences of sarcopenia. J Nutr Health Aging 2009;13:708-712. ArticlePubMedPDF
  • 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.Article
  • 5. Fried LP, Guralnik JM. Disability in older adults: evidence regarding significance, etiology, and risk. J Am Geriatr Soc 1997;45:92-100. ArticlePubMed
  • 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;69:1244-1252. ArticlePubMed
  • 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;23:176-180. ArticlePubMedPDF
  • 8. Kim DJ. The epidemiology of diabetes in Korea. Diabetes Metab J 2011;35:303-308. ArticlePubMedPMC
  • 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;32:30-37.Article
  • 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;26:3257-3263. PubMed
  • 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;1:106-114. ArticlePubMed
  • 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-M377. ArticlePubMed
  • 13. Narayan KM, Boyle JP, Thompson TJ, Sorensen SW, Williamson DF. Lifetime risk for diabetes mellitus in the United States. JAMA 2003;290:1884-1890. ArticlePubMed
  • 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;82:872-878. ArticlePubMed
  • 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;76:473-481. ArticlePubMed
  • 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;147:755-763. ArticlePubMed
  • 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;12:249-256. ArticlePubMedPMC
  • 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;61:72-77. ArticlePubMed
  • 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;31:652-658. ArticlePubMed
  • 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;57:2224-2231. ArticlePubMed
  • 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;69:547-558. ArticlePubMedPMC
  • 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;28:1041-1047. ArticlePubMedPMCPDF
  • 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. ArticlePubMed
  • 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;33:1652-1654. ArticlePubMedPMCPDF
  • 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;4:63-69.Article
  • 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;30:1507-1512. PubMed
  • 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;32:1993-1997. ArticlePubMedPMCPDF
  • 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;28:2541-2542. PubMed
  • 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;14:585-592. ArticlePubMed
  • 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;35:1672-1679. ArticlePubMedPMCPDF
  • 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;61:769-775. ArticlePubMedPMCPDF
  • 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):115-121. Article
  • 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;33:1497-1499. PubMedPMC
  • 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;40:140-146. ArticlePubMedPMCPDF
  • 35. Morley JE, Malmstrom TK, Rodriguez-Manas L, Sinclair AJ. Frailty, sarcopenia and diabetes. J Am Med Dir Assoc 2014;15:853-859. ArticlePubMed
  • 36. von Haehling S, Morley JE, Anker SD. From muscle wasting to sarcopenia and myopenia: update 2012. J Cachexia Sarcopenia Muscle 2012;3:213-217. ArticlePubMedPMC
  • 37. Wang X, Hu Z, Hu J, Du J, Mitch WE. Insulin resistance accelerates muscle protein degradation: activation of the ubiquitin-proteasome pathway by defects in muscle cell signaling. Endocrinology 2006;147:4160-4168. ArticlePubMedPDF
  • 38. Lawrence JC Jr. mTOR-dependent control of skeletal muscle protein synthesis. Int J Sport Nutr Exerc Metab 2001;11:S177-S185. ArticlePubMed
  • 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;64:132-137. ArticlePubMed
  • 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;108:191-195. ArticlePubMedPDF
  • 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;111:1545-1552. ArticlePubMed
  • 42. Andreassen CS, Jakobsen J, Andersen H. Muscle weakness: a progressive late complication in diabetic distal symmetric polyneuropathy. Diabetes 2006;55:806-812. PubMed
  • 43. Andersen H, Stalberg E, Gjerstad MD, Jakobsen J. Association of muscle strength and electrophysiological measures of reinnervation in diabetic neuropathy. Muscle Nerve 1998;21:1647-1654. ArticlePubMed
  • 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. ArticlePubMed
  • 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;91:923-930. ArticlePubMedPMC
  • 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-M332. PubMed
  • 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;59:242-248. ArticlePubMed
  • 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;91:3024-3033. ArticlePubMedPDF
  • 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-M156. ArticlePubMed
  • 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;68:62-67. ArticlePubMed
  • 51. Fried LP, Walston J. Chapter 116, Frailty and failure to thrive. Principles of geriatric medicine and gerontology. 5th ed. New York: McGraw Hill; 2003. p. 1487-1502.
  • 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;99:673-679. ArticlePubMedPMC
  • 53. Hubbard RE, Andrew MK, Fallah N, Rockwood K. Comparison of the prognostic importance of diagnosed diabetes, co-morbidity and frailty in older people. Diabet Med 2010;27:603-606. ArticlePubMedPDF
  • 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;50:251-260. ArticlePubMedPDF
  • 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;29:171-179. ArticlePubMedPDF
  • 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.e1-851.e6. ArticlePubMed
  • 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;27:423-447. ArticlePubMed
  • 58. Frankel JE, Bean JF, Frontera WR. Exercise in the elderly: research and clinical practice. Clin Geriatr Med 2006;22:239-256. viiArticlePubMed
  • 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-E101. ArticlePubMed
  • 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;53:260-266. ArticlePubMedPDF
  • 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;78:334-340. ArticlePubMed
  • 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;64:1038-1044. ArticlePubMed
  • 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;47:1208-1214. ArticlePubMed
  • 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;61:589-593. ArticlePubMed
  • 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;87:150-155. ArticlePubMed
  • 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;62:30-39. ArticlePubMed
  • 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-M380. ArticlePubMed
  • 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;89:731-739. ArticlePubMed
  • 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):CD003288ArticlePubMedPMC
Fig. 1

Changes of appendicular skeletal muscle mass (ASM), and ASM indices according to age trends in Korean (A) men and (B) women using data from Korea National Health and Nutrition Examination Study 2008 to 2010. ht2, height squared (m). Modified from Kim et al. [4].

dmj-40-182-g001.jpg
Table 1

Major causes or mechanisms of sarcopenia in older adults

dmj-40-182-i001.jpg
Primary Age related: sex hormones, muscle apoptosis, mitochondrial dysfunction
Secondary Activity related: physical inactivity, disuse, decon ditioning, zero gravity
Nutrition related: inadequate dietary intake, malabsorption, gastrointestinal disorders or medications that cause anorexia
Endocrine disorder related: obesity, insulin resistance, inflammatory cytokine, steroid treatment, abnormal thyroid function
Neurodegenerative disorder related: stroke, parkinsonism, diabetic neuropathy
Chronic disease related: malignancy, advanced organ failure
Table 2

Clinical phenotype of frailty proposed by Fried et al.

dmj-40-182-i002.jpg
Weight loss Unintentional loss of ≥4.5 kg in the past year
Weakness Hand-grip strength in the lowest 20% quintile adjusted for sex and body mass index
Exhaustion Poor endurance and energy, self-reported from the Center for Epidemiologic Studies Depression Scale
Slowness Walking speed under the lowest quintile adjusted for sex and height
Low physical activity level Lowest quintile of kilocalories of physical activity during the past week, measured by the Minnesota Leisure Activity Scale

Modified from Fried et al., with permission from Oxford University Press [49].

Figure & Data

References

    Citations

    Citations to this article as recorded by  
    • Glycemic control and prescription profiles in internal medicine inpatients: The role of frailty
      Jose Carlos Arévalo Lorido, Juana Carretero Gomez, Patricia Vazquez Rodriguez, Ricardo Gómez Huelgas, Carmen Marín Silvente, Fernando Javier Sánchez Lora, Elena Isaba Ares, Anna Pardo i Pelegrín, Onán Pérez Hernández, Javier Ena
      European Journal of Internal Medicine.2024; 121: 103.     CrossRef
    • Prolonged hospitalization and 1-year mortality are associated with sarcopenia and malnutrition in older patients with type 2 diabetes: A prospective cohort study
      Mileni Vanti Beretta, Tatiana Pedroso de Paula, Ticiana da Costa Rodrigues, Thais Steemburgo
      Diabetes Research and Clinical Practice.2024; 207: 111063.     CrossRef
    • The role of genes and myokines of developing sarcopenia: A review
      Farida V. Valeeva, Zhanna A. Rodygina, Tatyana S. Yilmaz
      Consilium Medicum.2024; 26(4): 219.     CrossRef
    • Effect of Frailty on Depression among Patients with Late-life Depression: A Test of Anger, Anxiety, and Resilience as Mediators
      Junhyung Kim, Hyun-Ghang Jeong, Moon-Soo Lee, Chi-Un Pae, Ashwin A. Patkar, Sang Won Jeon, Cheolmin Shin, Changsu Han
      Clinical Psychopharmacology and Neuroscience.2024; 22(2): 253.     CrossRef
    • Relationship Between Frailty and Diabetic Pharmacologic Therapy in Older Adults with Type 2 Diabetes: A Cross-Sectional Study
      Akiko Nishimura, Chie Masuda, Chiyo Murauchi, Miho Ishii, Yuko Murata, Terumi Kawasaki, Mayumi Azuma, Shin-ichi Harashima
      Drugs & Aging.2024;[Epub]     CrossRef
    • Urgent needs of caregiving in ageing populations with Alzheimer’s disease and other chronic conditions: Support our loved ones
      John W. Culberson, Jonathan Kopel, Ujala Sehar, P. Hemachandra Reddy
      Ageing Research Reviews.2023; 90: 102001.     CrossRef
    • Hand grip strength: A reliable assessment tool of frailty status on the person with type 2 diabetes mellitus
      Diogo Ramalho, Leonor Silva, Catarina Almeida, Luís Rocha, Gustavo Rocha, Rafaela Veríssimo
      Nutrition Clinique et Métabolisme.2023; 37(1): 45.     CrossRef
    • Comprehensive review: Frailty in pancreas transplant candidates and recipients
      Ronald F. Parsons, Ekamol Tantisattamo, Wisit Cheungpasitporn, Arpita Basu, Yee Lu, Krista L. Lentine, Kenneth J. Woodside, Neeraj Singh, Joseph Scalea, Tarek Alhamad, Ty B. Dunn, Franco H. Cabeza Rivera, Sandesh Parajuli, Martha Pavlakis, Matthew Cooper
      Clinical Transplantation.2023;[Epub]     CrossRef
    • Development and validation of a risk prediction model for frailty in patients with diabetes
      Fan Bu, Xiao-hui Deng, Na-ni Zhan, Hongtao Cheng, Zi-lin Wang, Li Tang, Yu Zhao, Qi-yuan Lyu
      BMC Geriatrics.2023;[Epub]     CrossRef
    • Amino Acid Profiles in Older Adults with Frailty: Secondary Analysis from MetaboFrail and BIOSPHERE Studies
      Riccardo Calvani, Anna Picca, Leocadio Rodriguez-Mañas, Matteo Tosato, Hélio José Coelho-Júnior, Alessandra Biancolillo, Olga Laosa, Jacopo Gervasoni, Aniello Primiano, Lavinia Santucci, Ottavia Giampaoli, Isabelle Bourdel-Marchasson, Sophie C. Regueme, A
      Metabolites.2023; 13(4): 542.     CrossRef
    • Where to Start? Physical Assessment, Readiness, and Exercise Recommendations for People With Type 1 or Type 2 Diabetes
      Marni Armstrong, Sheri R. Colberg, Ronald J. Sigal
      Diabetes Spectrum.2023; 36(2): 105.     CrossRef
    • The Association Between Sarcopenia and Diabetes: From Pathophysiology Mechanism to Therapeutic Strategy
      Huiling Chen, Xiaojing Huang, Meiyuan Dong, Song Wen, Ligang Zhou, Xinlu Yuan
      Diabetes, Metabolic Syndrome and Obesity.2023; Volume 16: 1541.     CrossRef
    • Analysis of Individual Components of Frailty in Simultaneous Pancreas and Kidney, and Solitary Pancreas Transplant Recipients
      Sandesh Parajuli, Jon Odorico, Isabel Breyer, Emily Zona, Fahad Aziz, Heather Lorden, Jacqueline Garonzik-Wang, Dixon Kaufman, Didier Mandelbrot
      Transplantation Direct.2023; 9(9): e1523.     CrossRef
    • Effects of moderate exercise versus light exercise on fasting blood glucose in obese patients with type 2 diabetes mellitus
      Manal Kamel Youssef
      Physiotherapy Quarterly.2023; 31(3): 101.     CrossRef
    • Risk factors associated with frailty in older adults with type 2 diabetes: A cross‐sectional study
      Chia‐Ling Lin, Neng‐Chun Yu, Hsueh‐Ching Wu, Yuan‐Ching Liu
      Journal of Clinical Nursing.2022; 31(7-8): 967.     CrossRef
    • Sarcopenia in patients with multiple sclerosis
      Hatice Yuksel, Mehtap Balaban, Ozlem Ozturk Tan, Semra Mungan
      Multiple Sclerosis and Related Disorders.2022; 58: 103471.     CrossRef
    • Amino acid profile of skeletal muscle loss in type 2 diabetes: Results from a 7-year longitudinal study in asians
      Serena Low, Jiexun Wang, Angela Moh, Su Fen Ang, Keven Ang, Yi-Ming Shao, Jianhong Ching, Hai Ning Wee, Lye Siang Lee, Jean-Paul Kovalik, Wern Ee Tang, Ziliang Lim, Tavintharan Subramaniam, Chee Fang Sum, Su Chi Lim
      Diabetes Research and Clinical Practice.2022; 186: 109803.     CrossRef
    • Assessment of Muscle Quantity, Quality and Function
      Bo Kyung Koo
      Journal of Obesity & Metabolic Syndrome.2022; 31(1): 9.     CrossRef
    • Sarcopenia is associated with cardiovascular risk in men with COPD, independent of adiposity
      Ah Young Leem, Young Sam Kim, Kung Soo Chung, Moo Suk Park, Young Ae Kang, Young-Mok Park, Ji Ye Jung
      Respiratory Research.2022;[Epub]     CrossRef
    • Decline in skeletal muscle mass is associated with cognitive decline in type 2 diabetes mellitus
      Serena Low, Kiat Sern Goh, Tze Pin Ng, Angela Moh, Su Fen Ang, Jonathon Khoo, Keven Ang, Philip Yap, Chin Yee Cheong, Wern Ee Tang, Ziliang Lim, Tavintharan Subramaniam, Chee Fang Sum, Su Chi Lim
      Journal of Diabetes and its Complications.2022; 36(9): 108258.     CrossRef
    • Frailty and diabetes in older adults: Overview of current controversies and challenges in clinical practice
      Mohd Zaquan Arif Abd.Ghafar, Mark O’Donovan, Duygu Sezgin, Elizabeth Moloney, Ángel Rodríguez-Laso, Aaron Liew, Rónán O’Caoimh
      Frontiers in Clinical Diabetes and Healthcare.2022;[Epub]     CrossRef
    • Implications of the Metabolic Control of Diabetes in Patients with Frailty Syndrome
      Marta Muszalik, Hubert Stępień, Grażyna Puto, Mateusz Cybulski, Donata Kurpas
      International Journal of Environmental Research and Public Health.2022; 19(16): 10327.     CrossRef
    • Protective Effect of Delta-Like 1 Homolog Against Muscular Atrophy in a Mouse Model
      Ji Young Lee, Minyoung Lee, Dong-Hee Lee, Yong-ho Lee, Byung-Wan Lee, Eun Seok Kang, Bong-Soo Cha
      Endocrinology and Metabolism.2022; 37(4): 684.     CrossRef
    • Diabetes and osteoporosis – Treating two entities: A challenge or cause for concern?
      Nicklas H. Rasmussen, Peter Vestergaard
      Best Practice & Research Clinical Rheumatology.2022; 36(3): 101779.     CrossRef
    • Predictors associated with prefrailty in older Taiwanese individuals with type 2 diabetes
      Shu-Fen Lee, Chih-Ping Li, Yen-Lin Chen, Dee Pei
      Medicine.2022; 101(38): e30432.     CrossRef
    • Association of walking speed with cognitive function in Chinese older adults: A nationally representative cohort study
      Jianping Liu, Kaiwang Cui, Qian Chen, Zhiteng Li, Jing Fu, Xiangwen Gong, Hui Xu
      Frontiers in Aging Neuroscience.2022;[Epub]     CrossRef
    • Lower insulin level is associated with sarcopenia in community-dwelling frail and non-frail older adults
      Yanxia Lu, Wee Shiong Lim, Xia Jin, Ma Schwe Zin Nyunt, Tamas Fulop, Qi Gao, Su Chi Lim, Anis Larbi, Tze Pin Ng
      Frontiers in Medicine.2022;[Epub]     CrossRef
    • Weight-adjusted waist index reflects fat and muscle mass in the opposite direction in older adults
      Nam Hoon Kim, Yousung Park, Nan Hee Kim, Sin Gon Kim
      Age and Ageing.2021; 50(3): 780.     CrossRef
    • Examining the links between regular leisure‐time physical activity, sitting time and prefrailty in community‐dwelling older adults
      Shu‐Hung Chang, Nai‐Hui Chien, Jackson Pui‐Man Wai, Ching‐Cheng Chiang, Ching‐Yi Yu
      Journal of Advanced Nursing.2021; 77(6): 2761.     CrossRef
    • Tale of the Frail: Understanding Frailty in Cirrhosis
      Faruq Pradhan, Natasha Narang, Michael Fallon
      Southern Medical Journal.2021; 114(3): 186.     CrossRef
    • Type 2 diabetes mellitus in older adults: clinical considerations and management
      Srikanth Bellary, Ioannis Kyrou, James E. Brown, Clifford J. Bailey
      Nature Reviews Endocrinology.2021; 17(9): 534.     CrossRef
    • Low Protein Intakes and Poor Diet Quality Associate with Functional Limitations in US Adults with Diabetes: A 2005–2016 NHANES Analysis
      Stephanie M. Fanelli, Owen J. Kelly, Jessica L. Krok-Schoen, Christopher A. Taylor
      Nutrients.2021; 13(8): 2582.     CrossRef
    • Yaşlı Diyabetik Hastalarda Malnutrisyonun Klinik Sonuçları ve Önemi
      Saadet KOÇ OKUDUR, Pinar SOYSAL
      OSMANGAZİ JOURNAL OF MEDICINE.2021;[Epub]     CrossRef
    • Combined Aerobic and Resistance Exercise Training Reduces Circulating Apolipoprotein J Levels and Improves Insulin Resistance in Postmenopausal Diabetic Women
      Yun Kyung Jeon, Sang Soo Kim, Jong Ho Kim, Hyun Jeong Kim, Hyun Jun Kim, Jang Jun Park, Yuen Suk Cho, So Hee Joung, Ji Ryang Kim, Bo Hyun Kim, Sang Heon Song, In Joo Kim, Yong Ki Kim, Young-Bum Kim
      Diabetes & Metabolism Journal.2020; 44(1): 103.     CrossRef
    • Effects of elastic band exercise on the frailty states in pre-frail elderly people
      Rujie Chen, Qingwen Wu, Dongyan Wang, Zhou Li, Howe Liu, Guangtian Liu, Ying Cui, Linlin Song
      Physiotherapy Theory and Practice.2020; 36(9): 1000.     CrossRef
    • Association between Lower Extremity Skeletal Muscle Mass and Impaired Cognitive Function in Type 2 Diabetes
      Serena Low, Tze Pin Ng, Chin Leong Lim, Angela Moh, Su Fen Ang, Jiexun Wang, Kiat Sern Goh, Keven Ang, Wern Ee Tang, Pek Yee Kwan, Tavintharan Subramaniam, Chee Fang Sum, Su Chi Lim
      Scientific Reports.2020;[Epub]     CrossRef
    • Low free triiodothyronine levels are associated with risk of frailty in older adults with type 2 diabetes mellitus
      Shuangling Xiu, Zhijing Mu, Lei Zhao, Lina Sun
      Experimental Gerontology.2020; 138: 111013.     CrossRef
    • The Biomechanics of Diabetes Mellitus and Limb Preservation
      Jonathan M. Labovitz, Dana Day
      Clinics in Podiatric Medicine and Surgery.2020; 37(1): 151.     CrossRef
    • Inorganic Arsenic Exposure Decreases Muscle Mass and Enhances Denervation-Induced Muscle Atrophy in Mice
      Chang-Mu Chen, Min-Ni Chung, Chen-Yuan Chiu, Shing-Hwa Liu, Kuo-Cheng Lan
      Molecules.2020; 25(13): 3057.     CrossRef
    • Physical Exercise and Myokines: Relationships with Sarcopenia and Cardiovascular Complications
      Sandra Maria Barbalho, Uri Adrian Prync Flato, Ricardo José Tofano, Ricardo de Alvares Goulart, Elen Landgraf Guiguer, Cláudia Rucco P. Detregiachi, Daniela Vieira Buchaim, Adriano Cressoni Araújo, Rogério Leone Buchaim, Fábio Tadeu Rodrigues Reina, Piero
      International Journal of Molecular Sciences.2020; 21(10): 3607.     CrossRef
    • The relationships between sarcopenic skeletal muscle loss during ageing and macronutrient metabolism, obesity and onset of diabetes
      Ailsa A. Welch, Richard P. G. Hayhoe, Donnie Cameron
      Proceedings of the Nutrition Society.2020; 79(1): 158.     CrossRef
    • Effects of low skeletal muscle mass and sarcopenic obesity on albuminuria: a 7-year longitudinal study
      Jee Hee Yoo, Gyuri Kim, Sung Woon Park, Min Sun Choi, Jiyeon Ahn, Sang-Man Jin, Kyu Yeon Hur, Moon-Kyu Lee, Mira Kang, Jae Hyeon Kim
      Scientific Reports.2020;[Epub]     CrossRef
    • Sarcopenia, nutritional status and type 2 diabetes mellitus: A cross‐sectional study in a group of Mexican women residing in a nursing home
      María C. Velázquez‐Alva, María E. Irigoyen‐Camacho, Marco A. Zepeda‐Zepeda, Irina Lazarevich, Isabel Arrieta‐Cruz, Carlos D'Hyver
      Nutrition & Dietetics.2020; 77(5): 515.     CrossRef
    • Assessing the association between optimal energy intake and all‐cause mortality in older patients with diabetes mellitus using the Japanese Elderly Diabetes Intervention Trial
      Takuya Omura, Yoshiaki Tamura, Takuya Yamaoka, Yukio Yoshimura, Takashi Sakurai, Hiroyuki Umegaki, Chiemi Kamada, Satoshi Iimuro, Yasuo Ohashi, Hideki Ito, Atsushi Araki
      Geriatrics & Gerontology International.2020; 20(1): 59.     CrossRef
    • Sarkopenie im Kontext von Insulinresistenz und Diabetes mellitus im Alter – Daten aus der Berliner Altersstudie II
      Dominik Spira, Nikolaus Buchmann, Knut Mai, Thomas Bobbert, Joachim Spranger, Ilja Demuth, Elisabeth Steinhagen-Thiessen
      Diabetologie und Stoffwechsel.2020; 15(05): 400.     CrossRef
    • Effect of Dietary Silk Peptide on Obesity, Hyperglycemia, and Skeletal Muscle Regeneration in High-Fat Diet-Fed Mice
      Kippeum Lee, Heegu Jin, Sungwoo Chei, Hyun-Ji Oh, Jeong-Yong Lee, Boo-Yong Lee
      Cells.2020; 9(2): 377.     CrossRef
    • Nutrition Management in Older Adults with Diabetes: A Review on the Importance of Shifting Prevention Strategies from Metabolic Syndrome to Frailty
      Yoshiaki Tamura, Takuya Omura, Kenji Toyoshima, Atsushi Araki
      Nutrients.2020; 12(11): 3367.     CrossRef
    • Mechanical Properties of Single Muscle Fibers: Understanding Poor Muscle Quality in Older Adults with Diabetes
      Eun-Jeong Lee, Hak Chul Jang, Kyung-Hoi Koo, Hye-Young Kim, Jae-Young Lim
      Annals of Geriatric Medicine and Research.2020; 24(4): 267.     CrossRef
    • Mortality is not increased with Diabetes in hospitalised very old adults: a multi-site review
      Peter Smerdely
      BMC Geriatrics.2020;[Epub]     CrossRef
    • Falls and Fractures in Diabetes—More than Bone Fragility
      Nicklas Højgaard Rasmussen, Jakob Dal
      Current Osteoporosis Reports.2019; 17(3): 147.     CrossRef
    • Measuring gait speed to better identify prodromal dementia
      Giulia Grande, Federico Triolo, Arturo Nuara, Anna-Karin Welmer, Laura Fratiglioni, Davide L. Vetrano
      Experimental Gerontology.2019; 124: 110625.     CrossRef
    • Diabetes and Muscle Dysfunction in Older Adults
      Hak Chul Jang
      Annals of Geriatric Medicine and Research.2019; 23(4): 160.     CrossRef
    • Association between sarcopenia and diabetes in community dwelling elderly in the Amazon region – Viver Mais Project
      Anelza Biene Farias Souza, David Anchieta Costa Nascimento, Isabella Juliana Manfredo Rodrigues, Cynthia Cillene Oliveira Charone, Geovanna Lemos Lopes, Rondinei Silva Lima, Ana Amália Sá, Thiago Xavier Carneiro, Niele Silva Moraes
      Archives of Gerontology and Geriatrics.2019; 83: 121.     CrossRef
    • Association between deterioration in muscle strength and peripheral neuropathy in people with diabetes
      Tae Jung Oh, Sunyoung Kang, Jie-Eun Lee, Jae Hoon Moon, Sung Hee Choi, Soo Lim, Hak Chul Jang
      Journal of Diabetes and its Complications.2019; 33(8): 598.     CrossRef
    • Frailty and Disability in Diabetes
      Sol-Ji Yoon, Kwang-il Kim
      Annals of Geriatric Medicine and Research.2019; 23(4): 165.     CrossRef
    • Mechanisms Involved in Glycemic Control Promoted by Exercise in Diabetics
      Eric Francelino Andrade, Víviam de Oliveira Silva, Débora Ribeiro Orlando, Luciano José Pereira
      Current Diabetes Reviews.2019; 15(2): 105.     CrossRef
    • Response: The Differential Association between Muscle Strength and Diabetes Mellitus According to the Presence or Absence of Obesity (J Obes Metab Syndr 2019;28:46-52)
      Bo Kyung Koo
      Journal of Obesity & Metabolic Syndrome.2019; 28(4): 297.     CrossRef
    • Diabetic Peripheral Neuropathy as a Risk Factor for Sarcopenia
      Tae Jung Oh, Yoojung Song, Jae Hoon Moon, Sung Hee Choi, Hak Chul Jang
      Annals of Geriatric Medicine and Research.2019; 23(4): 170.     CrossRef
    • Sarcopenia and hospital-related outcomes in the old people: a systematic review and meta-analysis
      Yunli Zhao, Yunxia Zhang, Qiukui Hao, Meiling Ge, Birong Dong
      Aging Clinical and Experimental Research.2019; 31(1): 5.     CrossRef
    • The Differential Association between Muscle Strength and Diabetes Mellitus According to the Presence or Absence of Obesity
      Bo Kyung Koo
      Journal of Obesity & Metabolic Syndrome.2019; 28(1): 46.     CrossRef
    • Sarcopenia in elderly patients with type 2 diabetes mellitus: prevalence and related clinical factors
      Yuko Murata, Yoshiki Kadoya, Shoichi Yamada, Tokio Sanke
      Diabetology International.2018; 9(2): 136.     CrossRef
    • Assessment of lower extremity muscle mass, muscle strength, and exercise therapy in elderly patients with diabetes mellitus
      Takuo Nomura, Toshihiro Kawae, Hiroaki Kataoka, Yukio Ikeda
      Environmental Health and Preventive Medicine.2018;[Epub]     CrossRef
    • Diabetes Treatment in the Elderly: Incorporating Geriatrics, Technology, and Functional Medicine
      Willy Marcos Valencia, Diana Botros, Maria Vera-Nunez, Stuti Dang
      Current Diabetes Reports.2018;[Epub]     CrossRef
    • Psoas and paraspinous muscle index as a predictor of mortality in African American men with type 2 diabetes mellitus
      Mariana Murea, Leon Lenchik, Thomas C. Register, Gregory B. Russell, Jianzhao Xu, S. Carrie Smith, Donald W. Bowden, Jasmin Divers, Barry I. Freedman
      Journal of Diabetes and its Complications.2018; 32(6): 558.     CrossRef
    • Presence of Sarcopenia and Its Rate of Change Are Independently Associated with Long-term Mortality in Patients with Liver Cirrhosis
      Jae Yoon Jeong, Sanghyeok Lim, Joo Hyun Sohn, Jae Gon Lee, Dae Won Jun, Yongsoo Kim
      Journal of Korean Medical Science.2018;[Epub]     CrossRef
    • Comparison between Dual-Energy X-ray Absorptiometry and Bioelectrical Impedance Analyses for Accuracy in Measuring Whole Body Muscle Mass and Appendicular Skeletal Muscle Mass
      Seo Young Lee, Soyeon Ahn, Young Ji Kim, Myoung Jin Ji, Kyoung Min Kim, Sung Hee Choi, Hak Chul Jang, Soo Lim
      Nutrients.2018; 10(6): 738.     CrossRef
    • The association of low muscle mass with soluble receptor for advanced glycation end products (sRAGE): The Korean Sarcopenic Obesity Study (KSOS)
      Tae Nyun Kim, Man Sik Park, Eun Joo Lee, Hye Soo Chung, Hye Jin Yoo, Hyun Joo Kang, Wook Song, Sei Hyun Baik, Kyung Mook Choi
      Diabetes/Metabolism Research and Reviews.2018;[Epub]     CrossRef
    • Obesity paradox on the survival of elderly patients with diabetes: an AHAP-based study
      Ali Bijani, Robert G. Cumming, Seyed-Reza Hosseini, Masoumeh Yazdanpour, Mahdis Rahimi, Abbas Sahebian, Reza Ghadimi
      Journal of Diabetes & Metabolic Disorders.2018; 17(1): 45.     CrossRef
    • Effects of Seahorse Supplementation on Muscle Mass, Exercise Performance Abilities and the Related Blood Factors in Healthy Elderly Women
      Bae-jin LEE, Chan-ho PARK, Byeong-Hwan JEON
      JOURNAL OF FISHRIES AND MARINE SCIENCES EDUCATION.2018; 30(2): 409.     CrossRef
    • Frailty risk in hospitalised older adults with and without diabetes mellitus
      Deborah A. Lekan, Thomas P. McCoy
      Journal of Clinical Nursing.2018; 27(19-20): 3510.     CrossRef
    • Sarcopenia
      А.А. Пальцын
      ZHurnal «Patologicheskaia fiziologiia i eksperimental`naia terapiia».2018; (2()): 113.     CrossRef
    • Prevention of Falls and Frailty in Older Adults with Diabetes
      Helen P. Hazuda, Sara E. Espinoza
      Current Geriatrics Reports.2017; 6(3): 158.     CrossRef
    • Patterns and Predictors of Frailty Transitions in Older Men: The Osteoporotic Fractures in Men Study
      Lauren R. Pollack, Stephanie Litwack‐Harrison, Peggy M. Cawthon, Kristine Ensrud, Nancy E. Lane, Elizabeth Barrett‐Connor, Thuy‐Tien Dam
      Journal of the American Geriatrics Society.2017; 65(11): 2473.     CrossRef
    • Diabetic Neuropathy and Gait: A Review
      Uazman Alam, David R. Riley, Ravinder S. Jugdey, Shazli Azmi, Satyan Rajbhandari, Kristiaan D’Août, Rayaz A. Malik
      Diabetes Therapy.2017; 8(6): 1253.     CrossRef
    • Care of older people with diabetes
      Trisha Dunning
      Nursing Standard.2017; 32(3): 50.     CrossRef
    • Decreased Muscle Strength and Quality in Diabetes-Related Dementia
      Akito Tsugawa, Yusuke Ogawa, Naoto Takenoshita, Yoshitsugu Kaneko, Hirokuni Hatanaka, Eriko Jaime, Raita Fukasawa, Haruo Hanyu
      Dementia and Geriatric Cognitive Disorders Extra.2017; 7(3): 454.     CrossRef
    • Aging of the endocrine system and its potential impact on sarcopenia
      Giovanni Vitale, Matteo Cesari, Daniela Mari
      European Journal of Internal Medicine.2016; 35: 10.     CrossRef

    • PubReader PubReader
    • Cite this Article
      Cite this Article
      export Copy Download
      Close
      Download Citation
      Download a citation file in RIS format that can be imported by all major citation management software, including EndNote, ProCite, RefWorks, and Reference Manager.

      Format:
      • RIS — For EndNote, ProCite, RefWorks, and most other reference management software
      • BibTeX — For JabRef, BibDesk, and other BibTeX-specific software
      Include:
      • Citation for the content below
      Sarcopenia, Frailty, and Diabetes in Older Adults
      Diabetes Metab J. 2016;40(3):182-189.   Published online April 20, 2016
      Close
    • XML DownloadXML Download
    Figure
    Jang HC. Sarcopenia, Frailty, and Diabetes in Older Adults. Diabetes Metab J. 2016;40(3):182-189.
    Received: Feb 10, 2016; Accepted: Mar 05, 2016
    DOI: https://doi.org/10.4093/dmj.2016.40.3.182.

    Diabetes Metab J : Diabetes & Metabolism Journal
    Close layer