The role of obesity in sarcopenia and the optimal body composition to prevent against sarcopenia and obesity

Chaoran Liu, Keith Yu-Kin Cheng, Xin Tong, Wing-Hoi Cheung, Simon Kwoon-Ho Chow, Sheung Wai Law, Ronald Man Yeung Wong, Chaoran Liu, Keith Yu-Kin Cheng, Xin Tong, Wing-Hoi Cheung, Simon Kwoon-Ho Chow, Sheung Wai Law, Ronald Man Yeung Wong

Abstract

Background: Elderly people with low lean and high fat mass, are diagnosed with sarcopenic obesity (SO), and often have poor clinical outcomes. This study aimed to explore the relationship between obesity and sarcopenia, and the optimal proportion of fat and muscle for old individuals.

Methods: Participants aged 60 years or above were instructed to perform bioelectrical impedance analysis to obtain the muscle and fat indicators, and handgrip strength was also performed. Sarcopenia was diagnosed according to predicted appendicular skeletal muscle mass and function. Body mass index (BMI) and body fat percentage (BF%) were used to define obesity. The association of muscle and fat indicators were analyzed by Pearson's correlation coefficient. Pearson Chi-Square test was utilized to estimate odds ratios (OR) and 95% confidence intervals (CI) on the risk of sarcopenia according to obesity status.

Results: 1637 old subjects (74.8 ± 7.8 years) participated in this study. Not only fat mass, but also muscle indicators were positively correlated to BMI and body weight (p < 0.05). Absolute muscle and fat mass in different positions had positive associations (p < 0.05). Muscle mass and strength were negatively related to appendicular fat mass percentage (p < 0.05). When defined by BMI (OR = 0.69, 95% CI [0.56, 0.86]; p = 0.001), obesity was a protective factor for sarcopenia, whilst it was a risk factor when using BF% (OR = 1.38, 95% CI [1.13, 1.69]; p = 0.002) as the definition. The risk of sarcopenia reduced with the increase of BMI in both genders. It was increased with raised BF% in males but displayed a U-shaped curve for females. BF% 26.0-34.6% in old females and lower than 23.9% in old males are recommended for sarcopenia and obesity prevention.

Conclusion: Skeletal muscle mass had strong positive relationship with absolute fat mass but negative associations with the percentage of appendicular fat mass. Obesity was a risk factor of sarcopenia when defined by BF% instead of BMI. The management of BF% can accurately help elderly people prevent against both sarcopenia and obesity.

Keywords: aging; body fat percentage; body mass index; fat; muscle; sarcopenic obesity.

Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Copyright © 2023 Liu, Cheng, Tong, Cheung, Chow, Law and Wong.

Figures

Figure 1
Figure 1
The correlation between muscle and fat indicators and the differences between normal, sarcopenic, obese, and sarcopenic obese groups. In (A), the dark blue showed the strong positive correlation (correlation coefficient = 1), while the dark red showed the strong negative correlation (correlation coefficient = –1). Black cross was shown if there was no statistical significance (P > 0.05). The correlation coefficient was displayed in the lower half of the square. Female=0, male=1 for gender. (B, C) showed the differences of SMM and BFM in four groups according to BMI- and BF%-defined obesity. The post-hoc results were shown as a, b, c, d on the bars with same color; the results in groups with inconsistent letters were significantly different (P < 0.05). AFM%, arm fat mass percentage; LFM%, leg fat mass percentage; BF%, body fat percentage; TFM%, trunk fat mass percentage; BMI, body fat index; WHR, waist to hip ratio; LFM, leg fat mass; FMI, fat mass index; AFM, arm fat mass; BFM, body fat mass; TFM, trunk fat mass; AFFM%, arm fat-free mass percentage; LFFM%, leg fat-free mass percentage; SMI, skeletal muscle mass index; ASMI, appendicular skeletal muscle mass index; SMM, skeletal muscle mass; AFFM, arm fat-free mass; HGS, handgrip strength; LFFM, leg fat-free mass; N, normal group; S, only sarcopenic group; O, only obese group; SO, sarcopenic obese group.
Figure 2
Figure 2
Linear regression model to show the annual rate of ASMI and HGS decline in females with (blue) or without (red) obesity. (A, B) showed the changes of ASMI and HGS according to age in females with or without obesity when obesity defined by BMI ≥ 25 kg/m2. (C, D) showed the changes of the above variables when obesity defined by body fat percentage > 35% in female. All p-value of regression models is ≤ 0.05. F, female; O, obese; NO, non-obese; BMI, body mass index; BF%, body fat percentage; ASMI, appendicular skeletal muscle mass index; HGS, handgrip strength.
Figure 3
Figure 3
Linear regression model to show the annual rate of ASMI and HGS decline in males with (blue) or without (red) obesity. (A, B) showed the changes of ASMI and HGS according to age in males with or without obesity when obesity defined by BMI ≥ 25 kg/m2. (C, D) showed the changes of the above variables when obesity defined by body fat percentage > 27% in male. All p-value of regression models is < 0.05. M, male; O, obese; NO, non-obese; BMI, body mass index; BF%, body fat percentage; ASMI, appendicular skeletal muscle mass index; HGS, handgrip strength.
Figure 4
Figure 4
The risk of sarcopenia in males and females with different BMI and BF%. (A) showed that BMI was classified into 5 intervals based on the recommendation from WHO, the normal BMI (18.5–22.9) was regarded the reference group with OR=1.00. Blue points as OR values and blue shade as 95% CI represented male, and red represented female. (B) showed that BF% was classified into 5 intervals by quintile, the group with the lowest value of BF% was reference group. The specific interval of male (blue) was shown on the upper horizontal axis and female (red) on the lower horizontal axis.

References

    1. Michel J-P, Leonardi M, Martin M, Prina M. Who's report for the decade of healthy ageing 2021–30 sets the stage for globally comparable data on healthy ageing. Lancet Healthy Longevity (2021) 2(3):e121–e2. doi: 10.1016/s2666-7568(21)00002-7
    1. Lv Y, Mao C, Gao X, Ji JS, Kraus VB, Yin Z, et al. . The obesity paradox is mostly driven by decreased noncardiovascular disease mortality in the oldest old in China: A 20-year prospective cohort study. Nat Aging (2022) 2(5):389–96. doi: 10.1038/s43587-022-00201-3
    1. Piche ME, Tchernof A, Despres JP. Obesity phenotypes, diabetes, and cardiovascular diseases. Circ Res (2020) 126(11):1477–500. doi: 10.1161/CIRCRESAHA.120.316101
    1. Lee DH, Keum N, Hu FB, Orav EJ, Rimm EB, Willett WC, et al. . Predicted lean body mass, fat mass, and all cause and cause specific mortality in men: Prospective us cohort study. BMJ (2018) 362:k2575. doi: 10.1136/bmj.k2575
    1. Winter JE, MacInnis RJ, Wattanapenpaiboon N, Nowson CA. Bmi and all-cause mortality in older adults: A meta-analysis. Am J Clin Nutr (2014) 99(4):875–90. doi: 10.3945/ajcn.113.068122
    1. Liu C, Wong PY, Chung YL, Chow SK, Cheung WH, Law SW, et al. . Deciphering the "Obesity paradox" in the elderly: A systematic review and meta-analysis of sarcopenic obesity. Obes Rev (2022) 24(2):e13534. doi: 10.1111/obr.13534
    1. Prado CM, Siervo M, Mire E, Heymsfield SB, Stephan BC, Broyles S, et al. . A population-based approach to define body-composition phenotypes. Am J Clin Nutr (2014) 99(6):1369–77. doi: 10.3945/ajcn.113.078576
    1. Yeung SSY, Reijnierse EM, Pham VK, Trappenburg MC, Lim WK, Meskers CGM, et al. . Sarcopenia and its association with falls and fractures in older adults: A systematic review and meta-analysis. J Cachexia Sarcopenia Muscle (2019) 10(3):485–500. doi: 10.1002/jcsm.12411
    1. Liu P, Hao Q, Hai S, Wang H, Cao L, Dong B. Sarcopenia as a predictor of all-cause mortality among community-dwelling older people: A systematic review and meta-analysis. Maturitas (2017) 103:16–22. doi: 10.1016/j.maturitas.2017.04.007
    1. Chen LK, Woo J, Assantachai P, Auyeung TW, Chou MY, Iijima K, et al. . Asian Working group for sarcopenia: 2019 consensus update on sarcopenia diagnosis and treatment. J Am Med Dir Assoc (2020) 21(3):300–7.e2. doi: 10.1016/j.jamda.2019.12.012
    1. Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyère O, Cederholm T, et al. . Sarcopenia: Revised European consensus on definition and diagnosis. Age Ageing (2019) 48(1):16–31. doi: 10.1093/ageing/afy169
    1. Khongsri N, Tongsuntud S, Limampai P, Kuptniratsaikul V. The prevalence of sarcopenia and related factors in a community-dwelling elders Thai population. Osteoporos Sarcopenia (2016) 2(2):110–5. doi: 10.1016/j.afos.2016.05.001
    1. Macek P, Biskup M, Terek-Derszniak M, Stachura M, Krol H, Gozdz S, et al. . Optimal body fat percentage cut-off values in predicting the obesity-related cardiovascular risk factors: A cross-sectional cohort study. Diabetes Metab Syndr Obes (2020) 13:1587–97. doi: 10.2147/DMSO.S248444
    1. Padwal R, Leslie WD, Lix LM, Majumdar SR. Relationship among body fat percentage, body mass index, and all-cause mortality: A cohort study. Ann Intern Med (2016) 164(8):532–41. doi: 10.7326/M15-1181
    1. Zhang X, Xie X, Dou Q, Liu C, Zhang W, Yang Y, et al. . Association of sarcopenic obesity with the risk of all-cause mortality among adults over a broad range of different settings: A updated meta-analysis. BMC Geriatr (2019) 19(1):183. doi: 10.1186/s12877-019-1195-y
    1. Messa GAM, Piasecki M, Hurst J, Hill C, Tallis J, Degens H. The impact of a high-fat diet in mice is dependent on duration and age, and differs between muscles. J Exp Biol (2020) 223(Pt 6):jeb217117. doi: 10.1242/jeb.217117
    1. Batsis JA, Villareal DT. Sarcopenic obesity in older adults: Aetiology, epidemiology and treatment strategies. Nat Rev Endocrinol (2018) 14(9):513–37. doi: 10.1038/s41574-018-0062-9
    1. Cheng KY, Chow SK, Hung VW, Wong CH, Wong RM, Tsang CS, et al. . Diagnosis of sarcopenia by evaluating skeletal muscle mass by adjusted bioimpedance analysis validated with dual-energy X-ray absorptiometry. J Cachexia Sarcopenia Muscle (2021) 12(6):2163–73. doi: 10.1002/jcsm.12825
    1. Gao Q, Mei F, Shang Y, Hu K, Chen F, Zhao L, et al. . Global prevalence of sarcopenic obesity in older adults: A systematic review and meta-analysis. Clin Nutr (2021) 40(7):4633–41. doi: 10.1016/j.clnu.2021.06.009
    1. World Health Organization. Regional Office for the Western P . The Asia-pacific perspective: Redefining obesity and its treatment. Sydney: Health Communications Australia; (2000).
    1. Perna S, Peroni G, Faliva MA, Bartolo A, Naso M, Miccono A, et al. . Sarcopenia and sarcopenic obesity in comparison: Prevalence, metabolic profile, and key differences. a cross-sectional study in Italian hospitalized elderly. Aging Clin Exp Res (2017) 29(6):1249–58. doi: 10.1007/s40520-016-0701-8
    1. Kemmler W, von Stengel S, Engelke K, Sieber C, Freiberger E. Prevalence of sarcopenic obesity in Germany using established definitions: Baseline data of the Formosa study. Osteoporos Int (2016) 27(1):275–81. doi: 10.1007/s00198-015-3303-y
    1. Du Y, Wang X, Xie H, Zheng S, Wu X, Zhu X, et al. . Sex differences in the prevalence and adverse outcomes of sarcopenia and sarcopenic obesity in community dwelling elderly in East China using the awgs criteria. BMC Endocr Disord (2019) 19(1):109. doi: 10.1186/s12902-019-0432-x
    1. Picca A, Coelho-Junior HJ, Calvani R, Marzetti E, Vetrano DL. Biomarkers shared by frailty and sarcopenia in older adults: A systematic review and meta-analysis. Ageing Res Rev (2021) 73:101530. doi: 10.1016/j.arr.2021.101530
    1. Arner P, Bernard S, Appelsved L, Fu KY, Andersson DP, Salehpour M, et al. . Adipose lipid turnover and long-term changes in body weight. Nat Med (2019) 25(9):1385–9. doi: 10.1038/s41591-019-0565-5
    1. Macek P, Terek-Derszniak M, Biskup M, Krol H, Smok-Kalwat J, Gozdz S, et al. . Assessment of age-induced changes in body fat percentage and bmi aided by Bayesian modelling: A cross-sectional cohort study in middle-aged and older adults. Clin Interv Aging (2020) 15:2301–11. doi: 10.2147/CIA.S277171
    1. Sniderman AD, Bhopal R, Prabhakaran D, Sarrafzadegan N, Tchernof A. Why might south asians be so susceptible to central obesity and its atherogenic consequences? the adipose tissue overflow hypothesis. Int J Epidemiol (2007) 36(1):220–5. doi: 10.1093/ije/dyl245
    1. Choi S, Chon J, Lee SA, Yoo MC, Yun Y, Chung SJ, et al. . Central obesity is associated with lower prevalence of sarcopenia in older women, but not in men: A cross-sectional study. BMC Geriatr (2022) 22(1):406. doi: 10.1186/s12877-022-03102-7
    1. Takegahara Y, Yamanouchi K, Nakamura K, Nakano S, Nishihara M. Myotube formation is affected by adipogenic lineage cells in a cell-to-Cell contact-independent manner. Exp Cell Res (2014) 324(1):105–14. doi: 10.1016/j.yexcr.2014.03.021
    1. Bucci L, Yani SL, Fabbri C, Bijlsma AY, Maier AB, Meskers CG, et al. . Circulating levels of adipokines and igf-1 are associated with skeletal muscle strength of young and old healthy subjects. Biogerontology (2013) 14(3):261–72. doi: 10.1007/s10522-013-9428-5
    1. Donini LM, Pinto A, Giusti AM, Lenzi A, Poggiogalle E. Obesity or bmi paradox? beneath the tip of the iceberg. Front Nutr (2020) 7:53. doi: 10.3389/fnut.2020.00053
    1. Rossi AP, Urbani S, Fantin F, Nori N, Brandimarte P, Martini A, et al. . Worsening disability and hospitalization risk in sarcopenic obese and dynapenic abdominal obese: A 5.5 years follow-up study in elderly men and women. Front Endocrinol (Lausanne) (2020) 11:314. doi: 10.3389/fendo.2020.00314
    1. Roh E, Choi KM. Health consequences of sarcopenic obesity: A narrative review. Front Endocrinol (Lausanne) (2020) 11:332. doi: 10.3389/fendo.2020.00332
    1. Lechleitner M. Obesity and the metabolic syndrome in the elderly–a mini-review. Gerontology (2008) 54(5):253–9. doi: 10.1159/000161734
    1. Tekus E, Miko A, Furedi N, Rostas I, Tenk J, Kiss T, et al. . Body fat of rats of different age groups and nutritional states: Assessment by micro-ct and skinfold thickness. J Appl Physiol (1985) (2018) 124(2):268–75. doi: 10.1152/japplphysiol.00884.2016
    1. Goossens GH. The metabolic phenotype in obesity: Fat mass, body fat distribution, and adipose tissue function. Obes Facts (2017) 10(3):207–15. doi: 10.1159/000471488
    1. Batsis JA, Mackenzie TA, Bartels SJ, Sahakyan KR, Somers VK, Lopez-Jimenez F. Diagnostic accuracy of body mass index to identify obesity in older adults: Nhanes 1999-2004. Int J Obes (Lond) (2016) 40(5):761–7. doi: 10.1038/ijo.2015.243
    1. Koster A, Ding J, Stenholm S, Caserotti P, Houston DK, Nicklas BJ, et al. . Does the amount of fat mass predict age-related loss of lean mass, muscle strength, and muscle quality in older adults? J Gerontol A Biol Sci Med Sci (2011) 66(8):888–95. doi: 10.1093/gerona/glr070
    1. Chen CA, Lai MC, Huang H, Wu CE. Interventions for body composition and upper and lower extremity muscle strength in older adults in rural Taiwan: A horizontal case study. Int J Environ Res Public Health (2022) 19(13):7869. doi: 10.3390/ijerph19137869
    1. Lopez P, Taaffe DR, Galvao DA, Newton RU, Nonemacher ER, Wendt VM, et al. . Resistance training effectiveness on body composition and body weight outcomes in individuals with overweight and obesity across the lifespan: A systematic review and meta-analysis. Obes Rev (2022) 23(5):e13428. doi: 10.1111/obr.13428
    1. Rankin JW. Effective diet and exercise interventions to improve body composition in obese individuals. Am J Lifestyle Med (2013) 9(1):48–62. doi: 10.1177/1559827613507879
    1. Oh H, Coburn SB, Matthews CE, Falk RT, LeBlanc ES, Wactawski-Wende J, et al. . Anthropometric measures and serum estrogen metabolism in postmenopausal women: The women's health initiative observational study. Breast Cancer Res (2017) 19(1):28. doi: 10.1186/s13058-017-0810-0
    1. Geraci A, Calvani R, Ferri E, Marzetti E, Arosio B, Cesari M. Sarcopenia and menopause: The role of estradiol. Front Endocrinol (Lausanne) (2021) 12:682012. doi: 10.3389/fendo.2021.682012
    1. Kim KB, Shin YA. Males with obesity and overweight. J Obes Metab Syndr (2020) 29(1):18–25. doi: 10.7570/jomes20008

Source: PubMed

3
Se inscrever