Europe PMC

This website requires cookies, and the limited processing of your personal data in order to function. By using the site you are agreeing to this as outlined in our privacy notice and cookie policy.

Abstract 


The aging process is associated with progressive loss of muscle mass and strength, as well as decline in physical functioning. Although consensus diagnosis has not been reached, sarcopenia is increasingly defined by both loss of muscle mass and loss of muscle function or strength. The cause of sarcopenia is suggested as multifactorial, including hormonal changes, inflammatory pathway activation, fatty infiltration, poor nutrition, and decreased physical activity. Sarcopenia is often associated with visceral obesity. Sarcopenic obesity in the elderly impacts metabolic complications and represents a major public health challenge in a rapidly aging society. Further research about sarcopenia and sarcopenic obesity may be needed to confront the influence of aging society in Korea.

Free full text 


Logo of enmLink to Publisher's site
Endocrinol Metab (Seoul). 2013 Jun; 28(2): 86–89.
Published online 2013 Jun 18. https://doi.org/10.3803/EnM.2013.28.2.86
PMCID: PMC3811714
PMID: 24396659

Sarcopenia and Sarcopenic Obesity

Abstract

The aging process is associated with progressive loss of muscle mass and strength, as well as decline in physical functioning. Although consensus diagnosis has not been reached, sarcopenia is increasingly defined by both loss of muscle mass and loss of muscle function or strength. The cause of sarcopenia is suggested as multifactorial, including hormonal changes, inflammatory pathway activation, fatty infiltration, poor nutrition, and decreased physical activity. Sarcopenia is often associated with visceral obesity. Sarcopenic obesity in the elderly impacts metabolic complications and represents a major public health challenge in a rapidly aging society. Further research about sarcopenia and sarcopenic obesity may be needed to confront the influence of aging society in Korea.

Keywords: Sarcopenia, Obesity, Muscle

INTRODUCTION

Aging is associated with a progressive loss of muscle mass, quality and strength, which results in a condition known as sarcopenia. In 1989, Rosenberg and Roubenoff [1] proposed the term sarcopenia, originating from the Greek words sarx (flesh) and penia (loss). Sarcopenia has been defined as "the age-associated loss of skeletal muscle mass, which results in decreased strength and aerobic capacity and thus functional capacity" [2]. Lean muscle mass contributes up to 50% of total body weight in young adults but declines with age to 25% at 80 years old [3]. After 50 years of age, approximately 1% to 2% of muscle mass is expected to be lost per year, and muscle strength decreases at an even greater rate [4]. Sarcopenia is characterized by atrophy of type II muscle fiber and reduction in muscle fiber satellite cells with aging [5]. Interestingly, young men have twice as much muscle mass as fat mass, whereas this ratio is almost reversed in older men [6]. Aging is also related to increased visceral fat mass, which is an important factor in the development of metabolic syndrome, type 2 diabetes and cardiovascular disease. Sarcopenia and visceral obesity may have a synergistic impact on both chronic metabolic disorders and physical disability [7].

DEFINITION OF SARCOPENIA

Several different definitions of sarcopenia and sarcopenic obesity have been proposed in previous studies. Baumgartner et al. [8] defined sarcopenia as a two or greater standard deviation (SD) reduction in appendicular skeletal muscle (ASM) divided by height squared (ASM/height2) below the normal mean for a young reference group measured using dual X-ray absorptiometry [8]. Janssen et al. [9] proposed a definition of sarcopenia as skeletal muscle mass index (skeletal muscle mass [kg]/weight [kg]×100) one or two SD below the mean for a younger reference group. Newman et al. [10] introduced an alternative definition of sarcopenia, using appendicular lean mass adjusted for height and body fat mass (residuals). Recently, the European Working Group on Sarcopenia in Older People developed a practical clinical definition and recommends using the presence of both low muscle mass and low muscle function (strength or performance) for the diagnosis of sarcopenia [11]. Table 1 summarizes the measurement of muscle mass, strength, and function. The International Working Group on Sarcopenia proposed that a diagnosis of sarcopenia is consistent with a gait speed of less than 1 m/sec and an objectively measured low muscle mass (e.g., ASM mass relative to height2 that is ≤7.23 kg/m2 in men and ≤5.67 kg/m2 in women) [2].

Table 1

Measurements of Muscle Mass, Strength, and Function

An external file that holds a picture, illustration, etc.
Object name is enm-28-86-i001.jpg

aRecommended for clinical practice.

MECHANISMS OF SARCOPENIA

Changes in hormone levels

Aging is associated with changes in hormone levels, such as those of growth hormone (GH), insulin-like growth factor (IGF)-I, insulin, androgens, estrogens, and corticosteroids, all of which affect the anabolic and catabolic conditions for muscle protein metabolism [12]. Elderly people show a decrease in GH and IGF-I levels that is paralleled by changes in body composition [13]. Reduced testosterone and estrogen levels might cause decreased muscle mass as well as diminishing bone strength. Increased insulin resistance with aging is associated with augmentation of intramyocellular fat mass and loss of muscle function [12].

Inflammation

Cytokines play a pivotal role not only in muscle homeostasis, but also in the pathogenesis of clinical conditions characterized by alterations in protein metabolism [14]. An increase in proinflammatory cytokines, such as tumor necrosis factor (TNF)-α, interleukin (IL)-1β, and IL-6, results in muscle breakdown, which is caused by decreasing muscle protein synthesis and increasing myofibrillar protein degradation [15]. TNF-α induces nuclear factor-κB, which leads to increasing proteolysis by activating the ubiquitin-dependent proteolysis system. IL-6 is considered to be a catabolic cytokine due to its participation in the regulation of muscle protein turnover [14].

Other risk factors

Several previous studies have demonstrated that serum 25-hydroxyvitamin D (25(OH)D) levels are inversely correlated with various parameters of obesity [16]. 25(OH)D levels decrease longitudinally with aging [17]. Recently, we found that insulin resistance and 25(OH)D levels were independently associated with sarcopenic obesity in men, while insulin resistance and high sensitivity C-reactive protein were significant factors predicting sarcopenic obesity in women [18]. On the other hand, oxidative metabolism generates reactive oxygen species, which damage cell components, particularly mitochondria. Alterations to mtDNA increase with age in skeletal muscle and are affected by sarcopenia [19]. Another important factor in the regulation of skeletal muscle mass is myostatin, which suppresses differentiation and proliferation of myocytes [20]. Myostatin suppression may have therapeutic potential for improvement of sarcopenia [21].

INFLUENCE OF SARCOPENIA AND SARCOPENIC OBESITY

Previous studies have reported that sarcopenia is associated with risk of adverse outcomes, such as physical disability, poor quality of life, and death. In an early study by Baumgartner et al. [8], sarcopenia was significantly associated with a 3-fold to 4-fold increased risk of physical disability in both men and women [8]. They also reported a relationship between sarcopenia and falls in the previous year. After adjustment for other confounding factors, the odds ratio for falls was statistically significant in men at 2.58 (95% confidence interval [CI], 0.60 to 2.67) but not in women at 1.28 (95% CI, 0.60 to 2.67) [8]. In the Korean Sarcopenic Obesity Study (KSOS) of 810 subjects (414 patients with type 2 diabetes and 396 control subjects), we found that type 2 diabetes was independently associated with increased risk of sarcopenia [22]. Furthermore, we observed that sarcopenic obesity was associated with the risk of metabolic syndrome [23]. Park et al. [24] showed that type 2 diabetes is associated with excessive loss of skeletal muscle, and that older women with type 2 diabetes in the Health ABC cohort are at especially high risk for loss of skeletal muscle mass [24]. Recently, Lim et al. [25] found that sarcopenic obesity, defined by ASM/weight, was more closely associated with metabolic syndrome than either sarcopenia or obesity alone. In a study including 1,396 men and women aged 70 years and older, low arm muscle area was associated with an elevated mortality rate during an 8-year follow-up period (hazard ratio, 1.95; 95% CI, 1.25 to 2.00) [26]. Heitmann et al. [27] reported that lower levels of fat-free mass were associated with an increased risk of mortality among 787 men aged 60 years and older who were followed for 22 years. Recent studies suggest that subjects with less common body-size phenotypes, such as metabolically abnormal but normal weight or metabolically healthy obese, seem to be more prone or more resistant, respectively, to the development of obesity-associated metabolic disorders. We observed that low muscle mass might be a factor associated with different metabolic consequences according to body-size phenotype in the KSOS cohort [28].

CONCLUSIONS

Both sarcopenia and obesity are becoming major threats to aging society. The concept of sarcopenic obesity may help to elucidate the interrelationship between physical disability, metabolic disorders and mortality in the elderly population. More research about sarcopenia and sarcopenic obesity is needed to improve morbidity and mortality as consequences of rapidly aging society.

ACKNOWLEDGMENTS

This research was supported by the Basic Science Research Program, through the National Research Foundation of Korea, funded by the Ministry of Education, Science and Technology (2012006363) and by the Brain Korea 21 Project of the Ministry of Education and Human Resources Development, Republic of Korea (A102065-1011-1070100).

Footnotes

No potential conflict of interest relevant to this article was reported.

References

1. Rosenberg IH, Roubenoff R. Stalking sarcopenia. Ann Intern Med. 1995;123:727–728. [Abstract] [Google Scholar]
2. 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;12:249–256. [Europe PMC free article] [Abstract] [Google Scholar]
3. 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. [Abstract] [Google Scholar]
4. Ferrucci L, Guralnik JM, Buchner D, Kasper J, Lamb SE, Simonsick EM, Corti MC, Bandeen-Roche K, Fried LP. Departures from linearity in the relationship between measures of muscular strength and physical performance of the lower extremities: the Women's Health and Aging Study. J Gerontol A Biol Sci Med Sci. 1997;52:M275–M285. [Abstract] [Google Scholar]
5. Verdijk LB, Koopman R, Schaart G, Meijer K, Savelberg HH, van Loon LJ. Satellite cell content is specifically reduced in type II skeletal muscle fibers in the elderly. Am J Physiol Endocrinol Metab. 2007;292:E151–E157. [Abstract] [Google Scholar]
6. Cohn SH, Vartsky D, Yasumura S, Sawitsky A, Zanzi I, Vaswani A, Ellis KJ. Compartmental body composition based on total-body nitrogen, potassium, and calcium. Am J Physiol. 1980;239:E524–E530. [Abstract] [Google Scholar]
7. Stenholm S, Harris TB, Rantanen T, Visser M, Kritchevsky SB, Ferrucci L. Sarcopenic obesity: definition, cause and consequences. Curr Opin Clin Nutr Metab Care. 2008;11:693–700. [Europe PMC free article] [Abstract] [Google Scholar]
8. 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. [Abstract] [Google Scholar]
9. 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;50:889–896. [Abstract] [Google Scholar]
10. Newman AB, Kupelian V, Visser M, Simonsick E, Goodpaster B, Nevitt M, Kritchevsky SB, Tylavsky FA, Rubin SM, Harris TB Health ABC Study Investigators. Sarcopenia: alternative definitions and associations with lower extremity function. J Am Geriatr Soc. 2003;51:1602–1609. [Abstract] [Google Scholar]
11. 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. [Europe PMC free article] [Abstract] [Google Scholar]
12. Wang C, Bai L. Sarcopenia in the elderly: basic and clinical issues. Geriatr Gerontol Int. 2012;12:388–396. [Abstract] [Google Scholar]
13. Zadik Z, Chalew SA, McCarter RJ, Jr, Meistas M, Kowarski AA. The influence of age on the 24-hour integrated concentration of growth hormone in normal individuals. J Clin Endocrinol Metab. 1985;60:513–516. [Abstract] [Google Scholar]
14. Zoico E, Roubenoff R. The role of cytokines in regulating protein metabolism and muscle function. Nutr Rev. 2002;60:39–51. [Abstract] [Google Scholar]
15. 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–E347. [Abstract] [Google Scholar]
16. Baz-Hecht M, Goldfine AB. The impact of vitamin D deficiency on diabetes and cardiovascular risk. Curr Opin Endocrinol Diabetes Obes. 2010;17:113–119. [Abstract] [Google Scholar]
17. Perry HM, 3rd, Horowitz M, Morley JE, Patrick P, Vellas B, Baumgartner R, Garry PJ. Longitudinal changes in serum 25-hydroxyvitamin D in older people. Metabolism. 1999;48:1028–1032. [Abstract] [Google Scholar]
18. 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;78:525–532. [Abstract] [Google Scholar]
19. Hiona A, Leeuwenburgh C. The role of mitochondrial DNA mutations in aging and sarcopenia: implications for the mitochondrial vicious cycle theory of aging. Exp Gerontol. 2008;43:24–33. [Europe PMC free article] [Abstract] [Google Scholar]
20. McCroskery S, Thomas M, Maxwell L, Sharma M, Kambadur R. Myostatin negatively regulates satellite cell activation and self-renewal. J Cell Biol. 2003;162:1135–1147. [Europe PMC free article] [Abstract] [Google Scholar]
21. Lang T, Streeper T, Cawthon P, Baldwin K, Taaffe DR, Harris TB. Sarcopenia: etiology, clinical consequences, intervention, and assessment. Osteoporos Int. 2010;21:543–559. [Europe PMC free article] [Abstract] [Google Scholar]
22. 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. [Europe PMC free article] [Abstract] [Google Scholar]
23. Kim TN, Yang SJ, Yoo HJ, Lim KI, Kang HJ, Song W, Seo JA, Kim SG, Kim NH, Baik SH, Choi DS, Choi KM. Prevalence of sarcopenia and sarcopenic obesity in Korean adults: the Korean sarcopenic obesity study. Int J Obes (Lond) 2009;33:885–892. [Abstract] [Google Scholar]
24. 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. [Europe PMC free article] [Abstract] [Google Scholar]
25. 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. [Europe PMC free article] [Abstract] [Google Scholar]
26. Miller MD, Crotty M, Giles LC, Bannerman E, Whitehead C, Cobiac L, Daniels LA, Andrews G. Corrected arm muscle area: an independent predictor of long-term mortality in community-dwelling older adults? J Am Geriatr Soc. 2002;50:1272–1277. [Abstract] [Google Scholar]
27. Heitmann BL, Erikson H, Ellsinger BM, Mikkelsen KL, Larsson B. Mortality associated with body fat, fat-free mass and body mass index among 60-year-old swedish men-a 22-year follow-up. The study of men born in 1913. Int J Obes Relat Metab Disord. 2000;24:33–37. [Abstract] [Google Scholar]
28. Kim TN, Park MS, Yang SJ, Yoo HJ, Kang HJ, Song W, Seo JA, Kim SG, Kim NH, Baik SH, Choi DS, Choi KM. Body size phenotypes and low muscle mass: the Korean sarcopenic obesity study (KSOS) J Clin Endocrinol Metab. 2013;98:811–817. [Abstract] [Google Scholar]

Articles from Endocrinology and Metabolism are provided here courtesy of Korean Endocrinology Society

Citations & impact 


Impact metrics

Jump to Citations

Citations of article over time

Alternative metrics

Altmetric item for https://www.altmetric.com/details/6009620
Altmetric
Discover the attention surrounding your research
https://www.altmetric.com/details/6009620

Article citations


Go to all (54) article citations

Similar Articles 


To arrive at the top five similar articles we use a word-weighted algorithm to compare words from the Title and Abstract of each citation.