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Evaluation of Sarcopenia in Elderly Women of China
International Journal of Gerontology 11 (2017) 149e153
Contents lists available at ScienceDirect
International Journal of Gerontology journal homepage: www.ijge-online.com
Original Article
Evaluation of Sarcopenia in Elderly Women of China Lufang Chen, Jiaying Xia, Zherong Xu, Yue Chen, Yunmei Yang* Department of Geriatrics, First Affiliated Hospital, School of Medicine, Zhejiang University, 79 Qingchun Road, Hangzhou, Zhejiang, 310003, China
a r t i c l e i n f o
s u m m a r y
Article history: Received 14 January 2016 Received in revised form 25 March 2016 Accepted 29 April 2016 Available online 1 September 2017
Background: Sarcopenia is a continuous process defined as a decline in both muscle mass and strength, which is a common phenomenon among elders and has been linked to multiple adverse clinical consequences. Varieties of factors contribute to the occurrence of sarcopenia. In the present study, we aim to observe the prevalence of sarcopenia in elderly women of China, and examine the effects of aging on the body composition change in China older women. Methods: 177 participants included 35.6% young women and 44.4% elderly women took part in this study between February 2015 and August 2015. All volunteers took dual energy X-ray absorptiometry tests for body composition assessment and physical-performance tests for physical function assessment. Results: Elderly women had greater total fat mass (25.2 ± 6.9 vs 22.5 ± 5.9, P ¼ 0.008) and percentage fat mass (45.1 ± 7.3 vs 41.7 ± 5.5, P < 0.001) than those in the young women. However, appendicular lean mass (ALM) and ALM/Height2 did not show statistical significance between young and older women. In spite of an equal muscle mass between two groups, the muscle strength (hand-grip strength, HGS) and physical function decline were more rapidly developed in elderly women, compared with their young counterparts. Conclusion: Our findings suggested that both aging and menopause contributes to the decline of muscle strength and physical function rather primarily than the loss of muscle mass in the process of sarcopenia in Chinese older women. Hand-grip strength criteria is more sensitive to diagnose sarcopenia in elderly women of China. Copyright © 2017, Taiwan Society of Geriatric Emergency & Critical Care Medicine. Published by Elsevier Taiwan LLC. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/ licenses/by-nc-nd/4.0/).
Keywords: sarcopenia, elderly women, muscle mass, muscle strength, physical function
1. Introduction Aging is a common trend in both developed and developing countries.1 According to World Health Organization, the number of people aged 60 years or older was 600 million in the year 2000, and will reach 1.2 billion by the year 2025.2 Aging results in a progressive decline of skeletal muscle mass, function, and strength. The age-related process is known as sarcopenia.3 Sarcopenia is a disorder of advanced age, which has a close relationship with falls, physical disability, and increased mortality.4 According to a variety of researches, the cause of sarcopenia is multifactorial, including malnutrition, neurodegenerative diseases, chronic illnesses, and metabolic diseases, all those contribute to the development of sarcopenia.5 Body composition is changed greatly during postmenopausal period. In elderly women, reduced body activity and changes in
* Corresponding author. E-mail address: [email protected] (Y. Yang).
endogenous hormonal balance, such as estrogen levels decline, cause an increase of visceral fat mass, and a reduction of muscle mass as well as muscle strength.6 As a result, older women are more susceptible to present sarcopenia, as opposed to young women and men. Although the prevalence of sarcopenia in elderly women has been widely reported in Brazil,7 America,8 and Europe,9 fewer studies have focused on the effect of aging on the body composition change in Asian older women. Unlike European and American ones, the Asian population is thinner, and thus their body composition is different from those of Western population. Therefore, we aim to evaluate the body composition including the low muscle mass (reflected by appendicular lean mass) in elderly women of China. Dual energy X-ray absorptiometry (DXA) is a practical technique applied for distinguishing lean, fat, and bone mineral tissues,9 which has been used widely for assessment of changes in body composition. Moreover, DXA also provides measurements of lean mass (LM) for arms, legs and trunk. The sum of lean mass for arm and leg has been defined as appendicular lean mass (ALM), which
http://dx.doi.org/10.1016/j.ijge.2016.04.005 1873-9598/Copyright © 2017, Taiwan Society of Geriatric Emergency & Critical Care Medicine. Published by Elsevier Taiwan LLC. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
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had usually been divided by height squared to form relative ALM.10 The relative ALM two standard deviations below the data of young counterparts is one of the criteria to diagnose sarcopenia.11
parameters, including the calcium, cholesterol, triglyceride and albumin. 2.4. Body composition
2. Materials and methods
All women volunteers signed written informed consent in accordance with the guidelines of institution, and the research was approved by the Human Ethics Committee of the First Affiliated Hospital of Medical College, Zhejiang University, China.
Fan-beam dual energy X-ray absorptiometry (DXA; DiscoveryW, Hologic, Bedford, MA, USA) was applied to measure fat mass (FM), lean mass (LM), total body water (TBW), and basal metabolism rate (BMR). In addition, the body mass index (BMI) was calculated by dividing weight in kilograms by height in meters squared (kg/m2). Appendicular lean mass (ALM) was calculated by summing up lean mass for both arms and legs.
2.2. Patients information
2.5. Hand-grip strength test
114 elderly women with a mean age of 67.9 years, and 63 young women aged 33e40 years (mean age 39.1 years) (Patients received to physical examination, relatives of patients and medical staff) with no recorded tumor, metabolic diseases or other neurodegenerative diseases known to affect the musculoskeletal system) were recruited by public advertisement between February 2015 and August 2015 at the Department of Geriatrics, First Affiliated Hospital of Medical College, Zhejiang University (Fig. 1). The data calculated from young women were used as reference values to define cutoff values for appendicular lean mass (ALM).
Hand-grip strength was measured applying a hydraulic hand dynamometer (Jamar Preston, Jackson, MI, USA) with forearms in a neutral position, and elbows flexed to 90 . The participants were instructed to grip the device as much as possible, the dominant hand was tested three times and the highest kilogramme was recorded for the statistical analyses.
2.1. Ethical approval of studies and informed consent
2.3. Clinical and laboratory parameter analysis Body height and weight were measured via a stadiometer (Holtain, Crymych, UK) with participants barefoot and in light clothing. All blood samples were obtained from the antecubital vein in the morning, after fasting of over 8 h, and were subjected to analysis using the Beckman-Coulter HMX automated system (Beckman-Coulter, Brea, CA, USA) to analyze the biochemical blood
2.6. Physical function Physical-performance was measured using gait speed, standing balance, and a five times sit-to-stand test according to Short Physical Performance Battery (SPPB) protocol (www.grc.nia.nih. gov/branches/ledb/sppb/) developed by the National Institute on Aging.12 In gait speed test, a flat unobstructed course was identified in a clinic assessment room, and 2.4 m were marked out with tape. The participants were asked to walk at their normal pace to finish a distance of 2.4 m, the time to fulfill the test was recorded by a stopwatch. The gait speed was recorded as 2.4 m divided by time. In standing balance test, the participants were required to maintain
Fig. 1. Flow chart of participants selection.
Sarcopenia in Elderly Women of China
their feet in the positions included semi-tandem (heel of one foot parallel to the big toe of the other foot), tandem (heel of one foot in front of the other foot), and side-by-side for 10 s, respectively. In sitto-stand test, participants were asked to sit down on a chair with their legs apart and knees flexed to 90 , and put their hands on their hips. Then the trained nurses instructed participants to repeat standing up and sit down five times at a self-paced speed. The time to fulfill the test was recorded for the analyses. 2.7. Definition of sarcopenia In the present study, sarcopenia was defined depending on different criteria. First, we use hand-grip strength to evaluate sarcopenia, that is, females in different groups of BMI 2SD below the mean of the hand-grip strength in young reference group respectively. Females with BMI 20 kg/m2, 20.1e23 kg/m2, 23.1e26 kg/m2 and 26.1 kg/m2 corresponding to hand-grip strength cutoff value 13.1, 16.1, 17, and 18.8 kg, respectively. Within the some literature, sarcopenia was defined as low muscle mass. Two definitions were applied for low muscle mass: 1) ALM divided by height squared (ALM/Height2; kg/m2) 2SD below the mean of the young reference group.7 2) ALM was measured by using a linear regression model to take height and total fat mass into account.8 The difference between the actual measured ALM and the predicted value generated by regression model represents the residual. A positive residual means a relatively muscular individual, whereas the negative one indicates a relatively sarcopenic individual. The linear regression model is as follows: ALM (kg) ¼ 15.311 þ 16.141 height (m) þ 0.081 total fat mass (kg). The cutoff value for low muscle mass is 2SD below the mean residual of the young reference group. In our study, 2SD below the mean of young women's residual is 3.4. Thus, women with residual 3.4 were considered to have sarcopenia. 2.8. Statistical analysis The homogeneity of variances was verified using Bartlett's test. Independent-sample t-tests were then performed to compare the volunteers' characteristics, clinical and laboratory parameters, and body composition between elderly and young women. The relationship between sarcopenia and body composition was assessed applying multiple linear regression. c2-tests were used to measure differences among categorical variables. p 0.05 was considered to show a statistically significant result. The statistical analysis was conducted using the SPSS 17.0 (SPSS, USA). 3. Results The demographic and laboratory data of the whole sample are listed in Table 1. Basal metabolism rate and hand-grip strength were significantly lower in elderly women, while BMI, body fat and triglyceride were higher, compared with young women. However, no statistical significance exits in weight, height, cholesterol, albumin, calcium and total body water between two groups. In this study, 177 participants included 35.6% young women and 44.4% elderly women took part in. Elderly women had greater total fat mass (25.2 ± 6.9 vs 22.5 ± 5.9, P ¼ 0.008) and percentage fat mass (45.1 ± 7.3 vs 41.7 ± 5.5, P < 0.001) than young women. However, ALM and ALM/Height2 did not show statistical significance between young and older women (Table 2). Table 3 shows a comparison among three different methods applied to define sarcopenia (hand-grip strength, ALM/Height2 and regression residuals which take height and total fat mass into account). Using definition 1 (hand-grip strength), the prevalence of sarcopenia was higher in elderly women than young women (26.3%
151 Table 1 Clinical and demographic information on young and elderly women.
Age (years) Weight (kg) Height (m) BMI (kg/m2) Body fat mass (kg) Cholesterol (mg/dL) Triglyceride (mg/dL) HDL cholesterol (mg/dL) LDL cholesterol (mg/dL) Total body water (kg) Basal metabolism rate (kcal) Albumin (g/dL) Calcium (mmol/L) Hand-grip strength (kg)
Young women
Elderly women
P value
39.1 ± 2.4 54.0 ± 9.6 1.6 ± 0.05 21.4 ± 3.5 22.5 ± 5.9 4.2 ± 0.9 1.2 ± 0.7 1.3 ± 0.3 2.3 ± 0.7 28.2 ± 2.8 1199.0 ± 76.6 42.0 ± 5.3 2.2 ± 0.2 21.9 ± 3.7
67.9 ± 9.2 55.6 ± 8.9 1.57 ± 0.06 22.4 ± 2.9 25.2 ± 6.9 4.4 ± 1.0 1.5 ± 0.8 1.3 ± 0.4 2.5 ± 0.8 27.9 ± 3.9 1061.6 ± 122.6 40.0 ± 5.0 2.2 ± 0.2 18.9 ± 3.9
0.278 0.121 0.033 0.008 0.084 0.015 0.953 0.052 0.597 <0.001 0.081 0.450 <0.001
Notes: BMI, body mass index.
Table 2 Comparison of sarcopenic indices by menopause status.
Number (%) Hand-grip strength (kg) ALM (kg) ALM/Height2 (kg/m2) Total fat mass (kg) Total percentage fat (%)
Young women
Elderly women
P value
63 (35.6) 21.9 ± 3.7 12.2 ± 2.0 4.8 ± 0.7 22.5 ± 5.9 41.7 ± 5.5
114 (64.4) 18.9 ± 3.9 12.1 ± 2.6 4.9 ± 0.9 25.2 ± 6.9 45.1 ± 7.3
<0.001 0.940 0.502 0.008 <0.001
Notes: ALM, appendicular lean mass.
Table 3 Prevalence of sarcopenia using different methods.
Definition 1 Definition 2 Definition 3
Young women (%)
Elderly women (%)
P value
4.8 1.6 5.3
26.3 4.4 4.8
<0.005 0.581 0.884
Notes: Definition 1: Females with BMI 20 kg/m2, 20.1e23 kg/m2, 23.1e26 kg/m2 and 26.1 kg/m2 corresponding to hand-grip strength cutoff value 13.1, 16.1, 17, and 18.8 kg, respectively. Definition 2: Appendicular lean mass/height2 2SD below the mean of the young women group. Definition 3: The residuals for ALM 2SD below the mean of young women's residuals for ALM.
vs 4.8%, P < 0.005). When we used the ALM/Height2 method (definition 2), no statistical significance was observed in the prevalence of sarcopenia between elderly women and young women (4.4% vs 1.6%, P ¼ 0.581). Using the 2SD below the mean of young women's residuals for ALM (definition 3), the prevalence of sarcopenia in young and elderly women groups was higher than definition 2, but still don't has significant difference (5.3% and 4.8%, P ¼ 0.884). The results of physical function assessments including gait speed, standing balance, and five times sit-to-stand test are shown in Table 4. As expected, elderly women had slower usual gait speed compared with their young counterparts (0.98 ± 0.27 vs 1.23 ± 0.17 m/s, P < 0.001). In standing balance test, shorter time
Table 4 Assess physical function by different tests.
Gait speed (m/s) Standing balance test Semi-tandem (s) Tandem (s) Side-by-side (s) Sit-to-stand test (s)
Young women
Elderly women
P value
1.23 ± 0.17
0.98 ± 0.27
<0.001
9.6 9.3 9.7 6.8
± ± ± ±
1.2 1.9 0.7 1.5
8.6 7.1 9.7 9.4
± ± ± ±
2.7 3.7 1.2 2.7
<0.001 <0.001 0.8052 <0.001
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elderly women used in semi-tandem (8.6 ± 2.7 vs 9.6 ± 1.2 s, P < 0.001) and tandem (7.1 ± 3.7 vs 9.3 ± 1.9 s, P < 0.001) tests compared to young women, whereas no significant difference exits between two groups in side-by-side test (9.7 ± 1.2 vs 9.7 ± 0.7 s, P ¼ 0.8052). Sit-to-stand test results were slower for elderly women compared with young women (9.4 ± 2.7 vs 6.8 ± 1.5 s, P < 0.001). 4. Discussion Aging is associated with an accelerated loss of physiological functions, muscle mass and strength.13 Thanks to the decreasing in body estrogen level, women suffer a losing of muscle mass and strength at an earlier age (around the age of menopause) compared with men.14 According to a numerous number of researches, most elderly women are usually more obese, have bigger fat mass, and smaller appendicular lean mass (low muscle mass) than young women in Western countries.7 However, our study reported that elderly women in China had equal ALM with young women. This is the first study demonstrating that elderly women had no less low muscle mass compared with young women in Asia. The possible explanations are as follows: 1) the ethnic differences between Western and Asian female population, 2) the number of participants included in this study is relatively small, further studies need to be done to confirm the hypothesis. It is well known that the loss of muscle strength is always concurrent with the loss of muscle mass. However, the relationship between muscle mass and muscle strength is not linear, the strength decline is more rapidly developed than the muscle mass loss, which suggests a decline in muscle quality.15,16,31 In our research, hand-grip strength was significantly lower in elderly women compared with young women, regardless of no statistical significance existed in muscle mass loss between two groups. Estrogen insufficiency may contribute to the muscle strength decline resulting from menopause.17 It was reported that estrogen receptors (ER), such as ER a and ER b were existed in human skeletal muscles.18 ERs were activated not only by estrogen19 but also insulin-like growth factor-1 (IGF-1).20 The activated ERs play an important role in muscle strength by stimulating anabolic pathways and activating satellite cells.21 Unfortunately, both estrogen and IGF-1 decline after menopause, as a result, the number of activated ERs decreases in elderly women compared with young women, and thus affects the muscle strength. Aging not only associated with changing of body composition,7 muscle strength, but also a decline in physical function.22 Poor physical function usually has a close relationship with high risk of physical disability.23 Recently, physical function performance has been measured widely in men and women older than 65 years old.24 Our results indicated that accompany with the reduction of muscle strength, elderly women have reduced physical function (slower gait speed, poor standing balance, and longer time in sit-tostand test) compared with their young counterparts. Although the most influential factor for physical function decline in elderly women remains unclear, several factors contributing to it have been found. Among them, physical activity was reported to be a crucial factor related to physical function in old women.25 Physical activity was defined as movement driven by skeletal muscles that need energy consumption.26 Higher level of physical activity was associated with higher functional status in older age.27 Moreover, greater physical activity has a close relationship with a better body composition, such as higher lean body mass and lower fat mass.28 Higher fat mass exacerbates age-related physical disability.29,30 To sum up, reduced physical activity contributes to the decline of physical function in elderly women. Beside physical activity, muscle quality31 and muscle capacity31,32 should also be taken into
L. Chen et al.
account. Muscle capacity refers to the muscle mass responsible for executing physical functions in daily life,33 while muscle quality was defined as muscle capacity normalized for leg lean mass.34 Both of them decline during menopausal transition.32 Our study reported that despite having an equal muscle mass, young women appear to have higher physical function and better physical performance compared with elderly women, suggesting higher muscle quality and muscle capacity in young women. The present study is not without limitations. First, there was no objective measure to estimate hormone level in female volunteers. Further studies are required to measure estrogen level to find out the relationship between elderly women (postmenopausal) and sarcopenia. Second, the present study did not examine lifestyle factors, such as smoking, alcohol drinking and nutritional status, which might have potential confounding effects on muscle mass and strength. Third, the sample was composed of older Chinese women and thus the results cannot be extrapolated to other populations or be applied to men. Finally, the number of subjects involved in this study is relatively small, studies on large sample need to be done to confirm the hypothesis. In conclusion, our results have shown that elderly women in China had greater total fat mass and percentage of fat mass than young women. However, ALM and ALM/Height2 did not show statistical significance between young and older women. Despite having an equal muscle mass between two groups, the muscle strength and physical function decline were more rapidly developed in elderly women compared with their premenopausal counterparts. Although the number of participants included in this study was relatively small, further studies need to be done. Our findings initially showed the effects of aging on the body composition and physical function change in Chinese older women. Acknowledgment This work is supported by the National Key Clinical Specialty Program, Zhejiang Provincial Science and Technology Department's major Scientific research program (provincial governors foundation), Zhejiang Provincial Science and Technology Department's major Scientific research program (Science and Technology Department's public welfare Program). (No. 2013C33122). References 1. Akishita M, Ishii S, Kojima T, et al. Priorities of health care outcomes for the elderly. J Am Med Dir Assoc. 2013;14:479e484. 2. Janssen I. The epidemiology of sarcopenia. Clin Geriatr Med. 2011;27:355e363. 3. Thompson DD. Aging and sarcopenia. J Musculoskelet Neuronal Interact. 2008;7: 344e345. 4. Cawthon PM, Marshall LM, Michael Y, et al. Frailty in older men: prevalence, progression, and relationship with mortality. J Am Geriatr Soc. 2007;55: 1216e1223. 5. Walston JD. Sarcopenia in older adults. Curr Opin Rheumatol. 2012;24:623e627. 6. Maltais ML, Desroches J, Dionne IJ. Changes in muscle mass and strength after menopause. J Musculoskelet Neuronal Interact. 2009;9:186e197. 7. Oliveira RJ, Bottaro M, Júnior JT, et al. Identification of sarcopenic obesity in postmenopausal women: a cutoff proposal. Braz J Med Biol Res. 2011;44: 1171e1176. 8. Newman AB, Kupelian V, Visser M, et al. Sarcopenia: alternative definitions and associations with lower extremity function. J Am Geriatr Soc. 2003;51: 1602e1609. 9. Cruz-Jentoft AJ, Baeyens JP, Bauer JM, et al. Sarcopenia: European consensus on definition and diagnosis: report of the European working group on sarcopenia in older people. Age Ageing. 2010;39:412e423. 10. Tanko LB, Movsesyan L, Mouritzen U, et al. Appendicular lean tissue mass and the prevalence of sarcopenia among healthy women. Metabolism. 2002;51: 69e74. 11. Baumgartner RN, Koehler KM, Gallagher D, et al. Epidemiology of sarcopenia among the elderly in New Mexico. Am J Epidemiol. 1998;147:755e763. 12. Guralnik JM, Ferrucci L, Simonsick EM, et al. Lower-extremity function in persons over the age of 70 years as a predictor of subsequent disability. N Engl J Med. 1995;332:556e562.
Sarcopenia in Elderly Women of China 13. Lindle RS, Metter EJ, Lynch NA, et al. Age and gender comparisons of muscle strength in 654 women and men aged 20-93 yr. J Appl Physiol (1985). 1997;83: 1581e1587. 14. Phillips SK, Rook KM, Siddle NC, et al. Muscle weakness in women occurs at an earlier age than in men, but strength is preserved by hormone replacement therapy. Clin Sci (Lond). 1993;84:95e98. 15. Goodpaster BH, Park SW, Harris TB, et al. The loss of skeletal muscle strength, mass, and quality in older adults: the health, aging and body composition study. J Gerontol A Biol Sci Med Sci. 2006;61:1059e1064. 16. Janssen I, Baumgartner RN, Ross R, et al. Skeletal muscle cutpoints associated with elevated physical disability risk in older men and women. Am J Epidemiol. 2004;159:413e421. 17. Cooper R, Mishra G, Clennell S, et al. Menopausal status and physical performance in midlife: findings from a British birth cohort study. Menopause. 2008;15:1079e1085. 18. Wiik A, Ekman M, Johansson O, et al. Expression of both oestrogen receptor alpha and beta in human skeletal muscle tissue. Histochem Cell Biol. 2009;131: 181e189. 19. Diel P. The role of the estrogen receptor in skeletal muscle mass homeostasis and regeneration. Acta Physiol (Oxf). 2014;212:14e16. 20. Callewaert F, Sinnesael M, Gielen E, et al. Skeletal sexual dimorphism: relative contribution of sex steroids, GH-IGF1, and mechanical loading. J Endocrinol. 2010;207:127e134. 21. Velders M, Schleipen B, Fritzemeier KH, et al. Selective estrogen receptor-b activation stimulates skeletal muscle growth and regeneration. FASEB J. 2012;26:1909e1920. 22. Tseng LA, El Khoudary SR, Young EA, et al. The association of menopause status with physical function: the study of women's health across the nation. Menopause. 2012;19:1186e1192. 23. Nam S, Al Snih S, Markides K, et al. Lower body function as a predictor of mortality over 13 years of follow up: findings from hispanic established population for the epidemiological study of the elderly. Geriatr Gerontol Int. 2016;16:1324e1331.
153 24. Valentine RJ, Misic MM, Rosengren KS, et al. Sex impacts the relation between body composition and physical function in older adults. Menopause. 2009;16: 518e523. 25. van Lummel RC, Walgaard S, Pijnappels M, et al. Physical performance and physical activity in older adults: associated but separate domains of physical function in old age. PLoS One. 2015;10. e0144048. 26. Waxman A, World Health Assembly, World Health Organization. Global strategy on diet, physical activity and health. Food Nutr Bull. 2004;25:292e302. 27. Paterson DH, Warburton DE. Physical activity and functional limitations in older adults: a systematic review related to Canada's physical activity guidelines. Int J Behav Nutr Phys Act. 2010;7:38. 28. Asikainen T-M, Kukkonen-Harjula K, Miilunpalo S. Exercise for health for early postmenopausal women: a systematic review of randomized controlled trials. Sports Med. 2004;34:753e778. 29. Santanasto AJ, Newman AB, Strotmeyer ES, et al. Effects of changes in regional body composition on physical function in older adults: a pilot randomized controlled trial. J Nutr Health Aging. 2015;19:913e921. 30. Lebrun CE, van der Schouw YT, de Jong FH, et al. Fat mass rather than muscle strength is the major determinant of physical function and disability in postmenopausal women younger than 75 years of age. Menopause. 2006;13: 474e481. 31. Larson RD, Misic MM, Evans EM. Association of adiposity and muscle quality with physical function differs in young and old women. Menopause. 2015;22: 337e341. 32. Polotsky HN, Polotsky AJ. Metabolic implications of menopause. Semin Reprod Med. 2010;28:426e434. 33. Straight CR, Ward-Ritacco CL, Evans EM. Association between accelerometermeasured physical activity and muscle capacity in middle-aged postmenopausal women. Menopause. 2015;22:1204e1211. 34. Barbat-Artigas S, Rolland Y, Zamboni M, et al. How to assess functional status: a new muscle quality index. J Nutr Health Aging. 2012;16:67e77.
Contents lists available at ScienceDirect
International Journal of Gerontology journal homepage: www.ijge-online.com
Original Article
Evaluation of Sarcopenia in Elderly Women of China Lufang Chen, Jiaying Xia, Zherong Xu, Yue Chen, Yunmei Yang* Department of Geriatrics, First Affiliated Hospital, School of Medicine, Zhejiang University, 79 Qingchun Road, Hangzhou, Zhejiang, 310003, China
a r t i c l e i n f o
s u m m a r y
Article history: Received 14 January 2016 Received in revised form 25 March 2016 Accepted 29 April 2016 Available online 1 September 2017
Background: Sarcopenia is a continuous process defined as a decline in both muscle mass and strength, which is a common phenomenon among elders and has been linked to multiple adverse clinical consequences. Varieties of factors contribute to the occurrence of sarcopenia. In the present study, we aim to observe the prevalence of sarcopenia in elderly women of China, and examine the effects of aging on the body composition change in China older women. Methods: 177 participants included 35.6% young women and 44.4% elderly women took part in this study between February 2015 and August 2015. All volunteers took dual energy X-ray absorptiometry tests for body composition assessment and physical-performance tests for physical function assessment. Results: Elderly women had greater total fat mass (25.2 ± 6.9 vs 22.5 ± 5.9, P ¼ 0.008) and percentage fat mass (45.1 ± 7.3 vs 41.7 ± 5.5, P < 0.001) than those in the young women. However, appendicular lean mass (ALM) and ALM/Height2 did not show statistical significance between young and older women. In spite of an equal muscle mass between two groups, the muscle strength (hand-grip strength, HGS) and physical function decline were more rapidly developed in elderly women, compared with their young counterparts. Conclusion: Our findings suggested that both aging and menopause contributes to the decline of muscle strength and physical function rather primarily than the loss of muscle mass in the process of sarcopenia in Chinese older women. Hand-grip strength criteria is more sensitive to diagnose sarcopenia in elderly women of China. Copyright © 2017, Taiwan Society of Geriatric Emergency & Critical Care Medicine. Published by Elsevier Taiwan LLC. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/ licenses/by-nc-nd/4.0/).
Keywords: sarcopenia, elderly women, muscle mass, muscle strength, physical function
1. Introduction Aging is a common trend in both developed and developing countries.1 According to World Health Organization, the number of people aged 60 years or older was 600 million in the year 2000, and will reach 1.2 billion by the year 2025.2 Aging results in a progressive decline of skeletal muscle mass, function, and strength. The age-related process is known as sarcopenia.3 Sarcopenia is a disorder of advanced age, which has a close relationship with falls, physical disability, and increased mortality.4 According to a variety of researches, the cause of sarcopenia is multifactorial, including malnutrition, neurodegenerative diseases, chronic illnesses, and metabolic diseases, all those contribute to the development of sarcopenia.5 Body composition is changed greatly during postmenopausal period. In elderly women, reduced body activity and changes in
* Corresponding author. E-mail address: [email protected] (Y. Yang).
endogenous hormonal balance, such as estrogen levels decline, cause an increase of visceral fat mass, and a reduction of muscle mass as well as muscle strength.6 As a result, older women are more susceptible to present sarcopenia, as opposed to young women and men. Although the prevalence of sarcopenia in elderly women has been widely reported in Brazil,7 America,8 and Europe,9 fewer studies have focused on the effect of aging on the body composition change in Asian older women. Unlike European and American ones, the Asian population is thinner, and thus their body composition is different from those of Western population. Therefore, we aim to evaluate the body composition including the low muscle mass (reflected by appendicular lean mass) in elderly women of China. Dual energy X-ray absorptiometry (DXA) is a practical technique applied for distinguishing lean, fat, and bone mineral tissues,9 which has been used widely for assessment of changes in body composition. Moreover, DXA also provides measurements of lean mass (LM) for arms, legs and trunk. The sum of lean mass for arm and leg has been defined as appendicular lean mass (ALM), which
http://dx.doi.org/10.1016/j.ijge.2016.04.005 1873-9598/Copyright © 2017, Taiwan Society of Geriatric Emergency & Critical Care Medicine. Published by Elsevier Taiwan LLC. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
150
L. Chen et al.
had usually been divided by height squared to form relative ALM.10 The relative ALM two standard deviations below the data of young counterparts is one of the criteria to diagnose sarcopenia.11
parameters, including the calcium, cholesterol, triglyceride and albumin. 2.4. Body composition
2. Materials and methods
All women volunteers signed written informed consent in accordance with the guidelines of institution, and the research was approved by the Human Ethics Committee of the First Affiliated Hospital of Medical College, Zhejiang University, China.
Fan-beam dual energy X-ray absorptiometry (DXA; DiscoveryW, Hologic, Bedford, MA, USA) was applied to measure fat mass (FM), lean mass (LM), total body water (TBW), and basal metabolism rate (BMR). In addition, the body mass index (BMI) was calculated by dividing weight in kilograms by height in meters squared (kg/m2). Appendicular lean mass (ALM) was calculated by summing up lean mass for both arms and legs.
2.2. Patients information
2.5. Hand-grip strength test
114 elderly women with a mean age of 67.9 years, and 63 young women aged 33e40 years (mean age 39.1 years) (Patients received to physical examination, relatives of patients and medical staff) with no recorded tumor, metabolic diseases or other neurodegenerative diseases known to affect the musculoskeletal system) were recruited by public advertisement between February 2015 and August 2015 at the Department of Geriatrics, First Affiliated Hospital of Medical College, Zhejiang University (Fig. 1). The data calculated from young women were used as reference values to define cutoff values for appendicular lean mass (ALM).
Hand-grip strength was measured applying a hydraulic hand dynamometer (Jamar Preston, Jackson, MI, USA) with forearms in a neutral position, and elbows flexed to 90 . The participants were instructed to grip the device as much as possible, the dominant hand was tested three times and the highest kilogramme was recorded for the statistical analyses.
2.1. Ethical approval of studies and informed consent
2.3. Clinical and laboratory parameter analysis Body height and weight were measured via a stadiometer (Holtain, Crymych, UK) with participants barefoot and in light clothing. All blood samples were obtained from the antecubital vein in the morning, after fasting of over 8 h, and were subjected to analysis using the Beckman-Coulter HMX automated system (Beckman-Coulter, Brea, CA, USA) to analyze the biochemical blood
2.6. Physical function Physical-performance was measured using gait speed, standing balance, and a five times sit-to-stand test according to Short Physical Performance Battery (SPPB) protocol (www.grc.nia.nih. gov/branches/ledb/sppb/) developed by the National Institute on Aging.12 In gait speed test, a flat unobstructed course was identified in a clinic assessment room, and 2.4 m were marked out with tape. The participants were asked to walk at their normal pace to finish a distance of 2.4 m, the time to fulfill the test was recorded by a stopwatch. The gait speed was recorded as 2.4 m divided by time. In standing balance test, the participants were required to maintain
Fig. 1. Flow chart of participants selection.
Sarcopenia in Elderly Women of China
their feet in the positions included semi-tandem (heel of one foot parallel to the big toe of the other foot), tandem (heel of one foot in front of the other foot), and side-by-side for 10 s, respectively. In sitto-stand test, participants were asked to sit down on a chair with their legs apart and knees flexed to 90 , and put their hands on their hips. Then the trained nurses instructed participants to repeat standing up and sit down five times at a self-paced speed. The time to fulfill the test was recorded for the analyses. 2.7. Definition of sarcopenia In the present study, sarcopenia was defined depending on different criteria. First, we use hand-grip strength to evaluate sarcopenia, that is, females in different groups of BMI 2SD below the mean of the hand-grip strength in young reference group respectively. Females with BMI 20 kg/m2, 20.1e23 kg/m2, 23.1e26 kg/m2 and 26.1 kg/m2 corresponding to hand-grip strength cutoff value 13.1, 16.1, 17, and 18.8 kg, respectively. Within the some literature, sarcopenia was defined as low muscle mass. Two definitions were applied for low muscle mass: 1) ALM divided by height squared (ALM/Height2; kg/m2) 2SD below the mean of the young reference group.7 2) ALM was measured by using a linear regression model to take height and total fat mass into account.8 The difference between the actual measured ALM and the predicted value generated by regression model represents the residual. A positive residual means a relatively muscular individual, whereas the negative one indicates a relatively sarcopenic individual. The linear regression model is as follows: ALM (kg) ¼ 15.311 þ 16.141 height (m) þ 0.081 total fat mass (kg). The cutoff value for low muscle mass is 2SD below the mean residual of the young reference group. In our study, 2SD below the mean of young women's residual is 3.4. Thus, women with residual 3.4 were considered to have sarcopenia. 2.8. Statistical analysis The homogeneity of variances was verified using Bartlett's test. Independent-sample t-tests were then performed to compare the volunteers' characteristics, clinical and laboratory parameters, and body composition between elderly and young women. The relationship between sarcopenia and body composition was assessed applying multiple linear regression. c2-tests were used to measure differences among categorical variables. p 0.05 was considered to show a statistically significant result. The statistical analysis was conducted using the SPSS 17.0 (SPSS, USA). 3. Results The demographic and laboratory data of the whole sample are listed in Table 1. Basal metabolism rate and hand-grip strength were significantly lower in elderly women, while BMI, body fat and triglyceride were higher, compared with young women. However, no statistical significance exits in weight, height, cholesterol, albumin, calcium and total body water between two groups. In this study, 177 participants included 35.6% young women and 44.4% elderly women took part in. Elderly women had greater total fat mass (25.2 ± 6.9 vs 22.5 ± 5.9, P ¼ 0.008) and percentage fat mass (45.1 ± 7.3 vs 41.7 ± 5.5, P < 0.001) than young women. However, ALM and ALM/Height2 did not show statistical significance between young and older women (Table 2). Table 3 shows a comparison among three different methods applied to define sarcopenia (hand-grip strength, ALM/Height2 and regression residuals which take height and total fat mass into account). Using definition 1 (hand-grip strength), the prevalence of sarcopenia was higher in elderly women than young women (26.3%
151 Table 1 Clinical and demographic information on young and elderly women.
Age (years) Weight (kg) Height (m) BMI (kg/m2) Body fat mass (kg) Cholesterol (mg/dL) Triglyceride (mg/dL) HDL cholesterol (mg/dL) LDL cholesterol (mg/dL) Total body water (kg) Basal metabolism rate (kcal) Albumin (g/dL) Calcium (mmol/L) Hand-grip strength (kg)
Young women
Elderly women
P value
39.1 ± 2.4 54.0 ± 9.6 1.6 ± 0.05 21.4 ± 3.5 22.5 ± 5.9 4.2 ± 0.9 1.2 ± 0.7 1.3 ± 0.3 2.3 ± 0.7 28.2 ± 2.8 1199.0 ± 76.6 42.0 ± 5.3 2.2 ± 0.2 21.9 ± 3.7
67.9 ± 9.2 55.6 ± 8.9 1.57 ± 0.06 22.4 ± 2.9 25.2 ± 6.9 4.4 ± 1.0 1.5 ± 0.8 1.3 ± 0.4 2.5 ± 0.8 27.9 ± 3.9 1061.6 ± 122.6 40.0 ± 5.0 2.2 ± 0.2 18.9 ± 3.9
0.278 0.121 0.033 0.008 0.084 0.015 0.953 0.052 0.597 <0.001 0.081 0.450 <0.001
Notes: BMI, body mass index.
Table 2 Comparison of sarcopenic indices by menopause status.
Number (%) Hand-grip strength (kg) ALM (kg) ALM/Height2 (kg/m2) Total fat mass (kg) Total percentage fat (%)
Young women
Elderly women
P value
63 (35.6) 21.9 ± 3.7 12.2 ± 2.0 4.8 ± 0.7 22.5 ± 5.9 41.7 ± 5.5
114 (64.4) 18.9 ± 3.9 12.1 ± 2.6 4.9 ± 0.9 25.2 ± 6.9 45.1 ± 7.3
<0.001 0.940 0.502 0.008 <0.001
Notes: ALM, appendicular lean mass.
Table 3 Prevalence of sarcopenia using different methods.
Definition 1 Definition 2 Definition 3
Young women (%)
Elderly women (%)
P value
4.8 1.6 5.3
26.3 4.4 4.8
<0.005 0.581 0.884
Notes: Definition 1: Females with BMI 20 kg/m2, 20.1e23 kg/m2, 23.1e26 kg/m2 and 26.1 kg/m2 corresponding to hand-grip strength cutoff value 13.1, 16.1, 17, and 18.8 kg, respectively. Definition 2: Appendicular lean mass/height2 2SD below the mean of the young women group. Definition 3: The residuals for ALM 2SD below the mean of young women's residuals for ALM.
vs 4.8%, P < 0.005). When we used the ALM/Height2 method (definition 2), no statistical significance was observed in the prevalence of sarcopenia between elderly women and young women (4.4% vs 1.6%, P ¼ 0.581). Using the 2SD below the mean of young women's residuals for ALM (definition 3), the prevalence of sarcopenia in young and elderly women groups was higher than definition 2, but still don't has significant difference (5.3% and 4.8%, P ¼ 0.884). The results of physical function assessments including gait speed, standing balance, and five times sit-to-stand test are shown in Table 4. As expected, elderly women had slower usual gait speed compared with their young counterparts (0.98 ± 0.27 vs 1.23 ± 0.17 m/s, P < 0.001). In standing balance test, shorter time
Table 4 Assess physical function by different tests.
Gait speed (m/s) Standing balance test Semi-tandem (s) Tandem (s) Side-by-side (s) Sit-to-stand test (s)
Young women
Elderly women
P value
1.23 ± 0.17
0.98 ± 0.27
<0.001
9.6 9.3 9.7 6.8
± ± ± ±
1.2 1.9 0.7 1.5
8.6 7.1 9.7 9.4
± ± ± ±
2.7 3.7 1.2 2.7
<0.001 <0.001 0.8052 <0.001
152
elderly women used in semi-tandem (8.6 ± 2.7 vs 9.6 ± 1.2 s, P < 0.001) and tandem (7.1 ± 3.7 vs 9.3 ± 1.9 s, P < 0.001) tests compared to young women, whereas no significant difference exits between two groups in side-by-side test (9.7 ± 1.2 vs 9.7 ± 0.7 s, P ¼ 0.8052). Sit-to-stand test results were slower for elderly women compared with young women (9.4 ± 2.7 vs 6.8 ± 1.5 s, P < 0.001). 4. Discussion Aging is associated with an accelerated loss of physiological functions, muscle mass and strength.13 Thanks to the decreasing in body estrogen level, women suffer a losing of muscle mass and strength at an earlier age (around the age of menopause) compared with men.14 According to a numerous number of researches, most elderly women are usually more obese, have bigger fat mass, and smaller appendicular lean mass (low muscle mass) than young women in Western countries.7 However, our study reported that elderly women in China had equal ALM with young women. This is the first study demonstrating that elderly women had no less low muscle mass compared with young women in Asia. The possible explanations are as follows: 1) the ethnic differences between Western and Asian female population, 2) the number of participants included in this study is relatively small, further studies need to be done to confirm the hypothesis. It is well known that the loss of muscle strength is always concurrent with the loss of muscle mass. However, the relationship between muscle mass and muscle strength is not linear, the strength decline is more rapidly developed than the muscle mass loss, which suggests a decline in muscle quality.15,16,31 In our research, hand-grip strength was significantly lower in elderly women compared with young women, regardless of no statistical significance existed in muscle mass loss between two groups. Estrogen insufficiency may contribute to the muscle strength decline resulting from menopause.17 It was reported that estrogen receptors (ER), such as ER a and ER b were existed in human skeletal muscles.18 ERs were activated not only by estrogen19 but also insulin-like growth factor-1 (IGF-1).20 The activated ERs play an important role in muscle strength by stimulating anabolic pathways and activating satellite cells.21 Unfortunately, both estrogen and IGF-1 decline after menopause, as a result, the number of activated ERs decreases in elderly women compared with young women, and thus affects the muscle strength. Aging not only associated with changing of body composition,7 muscle strength, but also a decline in physical function.22 Poor physical function usually has a close relationship with high risk of physical disability.23 Recently, physical function performance has been measured widely in men and women older than 65 years old.24 Our results indicated that accompany with the reduction of muscle strength, elderly women have reduced physical function (slower gait speed, poor standing balance, and longer time in sit-tostand test) compared with their young counterparts. Although the most influential factor for physical function decline in elderly women remains unclear, several factors contributing to it have been found. Among them, physical activity was reported to be a crucial factor related to physical function in old women.25 Physical activity was defined as movement driven by skeletal muscles that need energy consumption.26 Higher level of physical activity was associated with higher functional status in older age.27 Moreover, greater physical activity has a close relationship with a better body composition, such as higher lean body mass and lower fat mass.28 Higher fat mass exacerbates age-related physical disability.29,30 To sum up, reduced physical activity contributes to the decline of physical function in elderly women. Beside physical activity, muscle quality31 and muscle capacity31,32 should also be taken into
L. Chen et al.
account. Muscle capacity refers to the muscle mass responsible for executing physical functions in daily life,33 while muscle quality was defined as muscle capacity normalized for leg lean mass.34 Both of them decline during menopausal transition.32 Our study reported that despite having an equal muscle mass, young women appear to have higher physical function and better physical performance compared with elderly women, suggesting higher muscle quality and muscle capacity in young women. The present study is not without limitations. First, there was no objective measure to estimate hormone level in female volunteers. Further studies are required to measure estrogen level to find out the relationship between elderly women (postmenopausal) and sarcopenia. Second, the present study did not examine lifestyle factors, such as smoking, alcohol drinking and nutritional status, which might have potential confounding effects on muscle mass and strength. Third, the sample was composed of older Chinese women and thus the results cannot be extrapolated to other populations or be applied to men. Finally, the number of subjects involved in this study is relatively small, studies on large sample need to be done to confirm the hypothesis. In conclusion, our results have shown that elderly women in China had greater total fat mass and percentage of fat mass than young women. However, ALM and ALM/Height2 did not show statistical significance between young and older women. Despite having an equal muscle mass between two groups, the muscle strength and physical function decline were more rapidly developed in elderly women compared with their premenopausal counterparts. Although the number of participants included in this study was relatively small, further studies need to be done. Our findings initially showed the effects of aging on the body composition and physical function change in Chinese older women. Acknowledgment This work is supported by the National Key Clinical Specialty Program, Zhejiang Provincial Science and Technology Department's major Scientific research program (provincial governors foundation), Zhejiang Provincial Science and Technology Department's major Scientific research program (Science and Technology Department's public welfare Program). (No. 2013C33122). References 1. Akishita M, Ishii S, Kojima T, et al. Priorities of health care outcomes for the elderly. J Am Med Dir Assoc. 2013;14:479e484. 2. Janssen I. The epidemiology of sarcopenia. Clin Geriatr Med. 2011;27:355e363. 3. Thompson DD. Aging and sarcopenia. J Musculoskelet Neuronal Interact. 2008;7: 344e345. 4. Cawthon PM, Marshall LM, Michael Y, et al. Frailty in older men: prevalence, progression, and relationship with mortality. J Am Geriatr Soc. 2007;55: 1216e1223. 5. Walston JD. Sarcopenia in older adults. Curr Opin Rheumatol. 2012;24:623e627. 6. Maltais ML, Desroches J, Dionne IJ. Changes in muscle mass and strength after menopause. J Musculoskelet Neuronal Interact. 2009;9:186e197. 7. Oliveira RJ, Bottaro M, Júnior JT, et al. Identification of sarcopenic obesity in postmenopausal women: a cutoff proposal. Braz J Med Biol Res. 2011;44: 1171e1176. 8. Newman AB, Kupelian V, Visser M, et al. Sarcopenia: alternative definitions and associations with lower extremity function. J Am Geriatr Soc. 2003;51: 1602e1609. 9. Cruz-Jentoft AJ, Baeyens JP, Bauer JM, et al. Sarcopenia: European consensus on definition and diagnosis: report of the European working group on sarcopenia in older people. Age Ageing. 2010;39:412e423. 10. Tanko LB, Movsesyan L, Mouritzen U, et al. Appendicular lean tissue mass and the prevalence of sarcopenia among healthy women. Metabolism. 2002;51: 69e74. 11. Baumgartner RN, Koehler KM, Gallagher D, et al. Epidemiology of sarcopenia among the elderly in New Mexico. Am J Epidemiol. 1998;147:755e763. 12. Guralnik JM, Ferrucci L, Simonsick EM, et al. Lower-extremity function in persons over the age of 70 years as a predictor of subsequent disability. N Engl J Med. 1995;332:556e562.
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