Abstract
Background
The objective was to determine if abdominal fat is related to poor muscle health.
Methods
This cross-sectional study included 428 males and 534 females with appendicular lean mass (ALM, kg) from dual-energy X-ray absorptiometry (DXA), grip strength (kg), and upper extremity muscle “quality” (grip strength/arm lean mass) measured (1996–2001) in the Framingham Offspring Study. Sex-specific linear regressions associated adiposity measures [waist circumference (WC, cm) and visceral adipose tissue (VAT, cm3), and subcutaneous adipose tissue (SAT, cm3)] as Z-scores with each measure of muscle, adjusting for covariates. Models were further stratified by body mass index (BMI, < 30, ≥ 30 kg/m2).
Results
Mean (± SD) age was 60 ± 9 years and BMI was 28.9 ± 4.6 kg/m2 (men) and 27.7 ± 5.8 kg/m2, (women). In men, the BMI-stratified analyses showed higher WC was associated with higher ALM (P < 0.0001 each) but with lower muscle quality (P < 0.02) in both BMI groups. Higher SAT was also associated with higher ALM (P = 0.0002) and lower muscle quality (P = 0.0002) in men with BMI < 30, but not in obese men. In women, higher WC, SAT, and VAT were each associated with higher ALM but lower muscle quality, particularly in obese women. Higher SAT (P = 0.05) and VAT (P = 0.04) were associated with higher quadriceps strength in women with BMI < 30 kg/m2 but not in obese women.
Conclusions
Higher abdominal fat may be associated with greater lean mass but poorer muscle quality, particularly in obese women. This suggests that adipose tissue may have endocrine influences on muscle, which should be confirmed in longitudinal studies.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs40520-023-02427-6/MediaObjects/40520_2023_2427_Fig1_HTML.png)
Similar content being viewed by others
Availability of data and materials
Data described in the manuscript, code book, and analytic code will be made available upon request pending application to and approval by the Framingham Heart Study.
References
United Nations, department of economic and social affairs, division. P. World population ageing 2019: highlights (ST/ESA/SER.A/430). 2019 2019. Report No.: 978-92-1-148325-3.
Janssen I (2010) Evolution of sarcopenia research. Appl Physiol Nutr Metab 35:707–712
Fielding RA, Vellas B, Evans WJ et al (2011) Sarcopenia: an undiagnosed condition in older adults. Current consensus definition: prevalence, etiology, and consequences. International working group on sarcopenia. J Am Med Dir Assoc 12:249–256
Bhasin S, Travison TG, Manini TM et al (2020) Sarcopenia definition: the position statements of the sarcopenia definition and outcomes consortium. J Am Geriatr Soc 68:1410–1418
Janssen I, Heymsfield SB, Ross R (2002) Low relative skeletal muscle mass (sarcopenia) in older persons is associated with functional impairment and physical disability. J Am Geriatr Soc 50:889–896
Cawthon PM, Manini T, Patel SM et al (2020) Putative cut-points in sarcopenia components and incident adverse health outcomes: an SDOC analysis. J Am Geriatr Soc 68:1429–1437
Janssen I, Shepard DS, Katzmarzyk PT et al (2004) The healthcare costs of sarcopenia in the United States. J Am Geriatr Soc 52:80–85
Ferrucci L, Penninx BW, Volpato S et al (2002) Change in muscle strength explains accelerated decline of physical function in older women with high interleukin-6 serum levels. J Am Geriatr Soc 50:1947–1954
Schaap LA, Pluijm SM, Deeg DJ et al (2009) Higher inflammatory marker levels in older persons: associations with 5-year change in muscle mass and muscle strength. J Gerontol A Biol Sci Med Sci 64:1183–1189
Visser M, Pahor M, Taaffe DR et al (2002) 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 57:M326–M332
Bucci L, Yani SL, Fabbri C et al (2013) Circulating levels of adipokines and IGF-1 are associated with skeletal muscle strength of young and old healthy subjects. Biogerontology 14:261–272
Brinkley TE, Leng X, Miller ME et al (2009) Chronic inflammation is associated with low physical function in older adults across multiple comorbidities. J Gerontol A Biol Sci Med Sci 64:455–461
Roubenoff R (2000) Sarcopenic obesity: does muscle loss cause fat gain? Lessons from rheumatoid arthritis and osteoarthritis. Ann N Y Acad Sci 904:553–557
Roubenoff R (2004) Sarcopenic obesity: the confluence of two epidemics. Obes Res 12:887–888
Schrager MA, Metter EJ, Simonsick E et al (2007) Sarcopenic obesity and inflammation in the InCHIANTI study. J Appl Physiol 102:919–925
Yokota T, Oritani K, Takahashi I et al (2000) Adiponectin, a new member of the family of soluble defense collagens, negatively regulates the growth of myelomonocytic progenitors and the functions of macrophages. Blood 96:1723–1732
Chiarugi P, Fiaschi T (2010) Adiponectin in health and diseases: from metabolic syndrome to tissue regeneration. Expert Opin Ther Targets 14:193–206
Havel PJ (2002) Control of energy homeostasis and insulin action by adipocyte hormones: leptin, acylation stimulating protein, and adiponectin. Curr Opin Lipidol 13:51–59
Stefan N, Vozarova B, Funahashi T et al (2002) Plasma adiponectin concentration is associated with skeletal muscle insulin receptor tyrosine phosphorylation, and low plasma concentration precedes a decrease in whole-body insulin sensitivity in humans. Diabetes 51:1884–1888
Yamauchi T, Kamon J, Minokoshi Y et al (2002) Adiponectin stimulates glucose utilization and fatty-acid oxidation by activating AMP-activated protein kinase. Nat Med 8:1288–1295
Karastergiou K, Smith SR, Greenberg AS et al (2012) Sex differences in human adipose tissues - the biology of pear shape. Biol Sex Differ 3:13
Pou KM, Massaro JM, Hoffmann U et al (2007) Visceral and subcutaneous adipose tissue volumes are cross-sectionally related to markers of inflammation and oxidative stress: the Framingham heart study. Circulation 116:1234–1241
Fox CS, Massaro JM, Hoffmann U et al (2007) Abdominal visceral and subcutaneous adipose tissue compartments: association with metabolic risk factors in the Framingham heart study. Circulation 116:39–48
Shuster A, Patlas M, Pinthus JH et al (2012) The clinical importance of visceral adiposity: a critical review of methods for visceral adipose tissue analysis. Br J Radiol 85:1–10
Karastergiou K, Fried SK (2013) Multiple adipose depots increase cardiovascular risk via local and systemic effects. Curr Atheroscler Rep 15:361
Ferrucci L, Alley D (2007) Obesity, disability, and mortality: a puzzling link. Arch Intern Med 167:750–751
Houston DK, Stevens J, Cai J (2005) Abdominal fat distribution and functional limitations and disability in a biracial cohort: the atherosclerosis risk in communities study. Int J Obes (Lond) 29:1457–1463
Cawthon PM, Fox KM, Gandra SR et al (2011) Clustering of strength, physical function, muscle, and adiposity characteristics and risk of disability in older adults. J Am Geriatr Soc 59:781–787
Angleman SB, Harris TB, Melzer D (2006) The role of waist circumference in predicting disability in periretirement age adults. Int J Obes (Lond) 30:364–373
Murphy RA, Reinders I, Register TC et al (2014) Associations of BMI and adipose tissue area and density with incident mobility limitation and poor performance in older adults. Am J Clin Nutr 99:1059–1065
Koster A, Ding J, Stenholm S et al (2011) 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 66:888–895
Wang H, Chen YE, Eitzman DT (2014) Imaging body fat: techniques and cardiometabolic implications. Arterioscler Thromb Vasc Biol 34:2217–2223
Bredella MA, Ghomi RH, Thomas BJ et al (2010) Comparison of DXA and CT in the assessment of body composition in premenopausal women with obesity and anorexia nervosa. Obesity (Silver Spring) 18:2227–2233
Kannel WB, Feinleib M, McNamara PM et al (1979) An investigation of coronary heart disease in families. The Framingham offspring study. Am J Epidemiol 110:281–290
Onuma OK, Pencina K, Qazi S et al (2017) Relation of risk factors and abdominal aortic calcium to progression of coronary artery calcium (from the Framingham heart study). Am J Cardiol 119:1584–1589
Onat A, Avci GS, Barlan MM et al (2004) Measures of abdominal obesity assessed for visceral adiposity and relation to coronary risk. Int J Obes Relat Metab Disord 28:1018–1025
Wang H, Troy LM, Rogers GT et al (2014) Longitudinal association between dairy consumption and changes of body weight and waist circumference: the Framingham heart study. Int J Obes (Lond) 38:299–305
Lee JJ, Pedley A, Hoffmann U et al (2016) Cross-sectional associations of computed tomography (CT)-derived adipose tissue density and adipokines: the Framingham heart study. J Am Heart Assoc 5:e002545
Visser M, Harris TB, Langlois J et al (1998) Body fat and skeletal muscle mass in relation to physical disability in very old men and women of the Framingham heart study. J Gerontol A Biol Sci Med Sci 53:M214–M221
Piao C, Yoshimoto N, Shitama H et al (2004) Validity and reliability of the measurement of the quardriceps femoris muscle strength with a hand-held dynamometer on the affected side in hemiplegic patients. J UOEH 26:1–11
Newman AB, Haggerty CL, Goodpaster B et al (2003) Strength and muscle quality in a well-functioning cohort of older adults: the health, aging and body composition study. J Am Geriatr Soc 51:323–330
Schnabel R, Larson MG, Dupuis J et al (2008) Relations of inflammatory biomarkers and common genetic variants with arterial stiffness and wave reflection. Hypertension 51:1651–1657
Frankel DS, Vasan RS, D’Agostino RB Sr et al (2009) Resistin, adiponectin, and risk of heart failure the Framingham offspring study. J Am Coll Cardiol 53:754–762
Benjamin EJ, Larson MG, Keyes MJ et al (2004) Clinical correlates and heritability of flow-mediated dilation in the community: the Framingham heart study. Circulation 109:613–619
MacKinnon DP, Krull JL, Lockwood CM (2000) Equivalence of the mediation, confounding and suppression effect. Prev Sci 1:173–181
Roubenoff R, Castaneda C (2001) Sarcopenia-understanding the dynamics of aging muscle. JAMA 286:1230–1231
Lim JP, Leung BP, Ding YY et al (2015) Monocyte chemoattractant protein-1: a proinflammatory cytokine elevated in sarcopenic obesity. Clin Interv Aging 10:605–609
Steppan CM, Bailey ST, Bhat S et al (2001) The hormone resistin links obesity to diabetes. Nature 409:307–312
Acknowledgements
Not applicable
Funding
Research reported in this publication was supported by the National Institute On Aging of the National Institutes of Health under Award Numbers R03AG053679 and R01 AG051728; the National Institute of Arthritis and Musculoskeletal and Skin Diseases (grant number R01 AR041398); the National Heart, Lung, and Blood Institute’s Framingham Heart Study (contract number HHSN268201500001I); the National Institute on Aging support of the Boston Claude D. Pepper Center Older American Independence Centers (grant number 1P30AG031679 to SS); and the MSTAR Training Grant (grant number NIA 5T35AG038027-09 (MPI) to RR). Any opinions, findings, conclusions, or recommendations expressed in this publication are those of the authors and do not necessarily reflect the official views of the National Institutes of Health.
Author information
Authors and Affiliations
Contributions
The authors’ responsibilities were as follows—RRM, MTH, and DPK obtained funding; RRM designed the research; SS analyzed data with critical input from all the co-authors; RM and SS drafted the manuscript with editing by all the authors; SS had primary responsibility for final content; and all the authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
Dr. Sahni reports institutional grants from Dairy Management Inc., Solarea Bio Inc., has reviewed grants for the American Egg Board’s Egg Nutrition Center and National Dairy Council, and she serves on a scientific advisory board for the Institute for the Advancement of Foods and Nutrition Sciences (IAFNS, unpaid position ended July 2022). Dr. Kiel has received grant funding to his institution from Amgen, Solarea Bio Inc., and Radius Health. He serves on the scientific advisory boards of Pfizer and Solarea Bio Inc. Dr. Hannan has received institutional grant funding from Amgen. Dr. Raghupathy and Dr. McLean have no relevant financial or non-financial interests to disclose related to this current work.
Research involving human participants and informed consent
This study was performed in accordance with the Declaration of Helsinki. All study participants gave informed consent for the parent Framingham Heart Study, which was approved by the IRB at Boston University. The current study utilized previously collected data and the protocol was approved by the Institutional Review Board (or Ethics Committee) of Advarra (Protocol #Pro00044485).
Consent to publication
Not applicable.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Raghupathy, R., McLean, R.R., Kiel, D.P. et al. Higher abdominal adiposity is associated with higher lean muscle mass but lower muscle quality in middle-aged and older men and women: the Framingham Heart Study. Aging Clin Exp Res 35, 1477–1485 (2023). https://doi.org/10.1007/s40520-023-02427-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40520-023-02427-6