Levels of Sex Hormones and Abdominal Muscle Composition in Men from The Multi-Ethnic Study of Atherosclerosis.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
12 Jul 2024
12 Jul 2024
Historique:
received:
29
01
2024
accepted:
05
07
2024
medline:
13
7
2024
pubmed:
13
7
2024
entrez:
12
7
2024
Statut:
epublish
Résumé
Information on the associations of testosterone levels with abdominal muscle volume and density in men is limited, while the role of estradiol and SHBG on these muscle characteristics are unclear. Therefore, this study aimed to investigate the association between fasting serum sex hormones and CT-derived abdominal muscle area and radiodensity in adult men. Conducted as a cross sectional observational study using data from the Multi-Ethnic Study of Atherosclerosis, our analyses focused on a community-based sample of 907 men aged 45-84 years, with 878 men having complete data. CT scans of the abdomen were interrogated for muscle characteristics, and multivariable linear regressions were used to test the associations. After adjustment for relevant factors, higher levels of both total testosterone and estradiol were associated with higher abdominal muscle area (1.74, 0.1-3.4, and 1.84, 0.4-3.3, respectively). In the final analyses, levels of total testosterone showed a positive association, while an inverse relationship was observed for SHBG with abdominal muscle radiodensity (0.3, 0.0-0.6, and - 0.33, - 0.6 to - 0.1, respectively). Our results indicate a complex association between sex hormones and abdominal muscle characteristics in men. Specifically, total testosterone and estradiol were associated with abdominal muscle area, while only total testosterone was associated with muscle radiodensity and SHBG was inversely associated with muscle radiodensity.Clinical Trial: NCT00005487.
Identifiants
pubmed: 38997435
doi: 10.1038/s41598-024-66948-4
pii: 10.1038/s41598-024-66948-4
doi:
Substances chimiques
Testosterone
3XMK78S47O
Estradiol
4TI98Z838E
Sex Hormone-Binding Globulin
0
Gonadal Steroid Hormones
0
Banques de données
ClinicalTrials.gov
['NCT00005487']
Types de publication
Journal Article
Observational Study
Langues
eng
Sous-ensembles de citation
IM
Pagination
16114Subventions
Organisme : VGR Regional Research and Development Council Grants
ID : ALFGBG-966255
Organisme : VGR Regional Research and Development Council Grants
ID : ALFGBG-966255
Organisme : NHLBI NIH HHS
ID : 75N92020D00001, HHSN268201500003I, N01-HC-95159, 75N92020D00005, N01-HC-95160, 75N92020D00002, N01-HC-95161, 75N92020D00003, N01-HC-95162, 75N92020D00006, N01-HC-95163, 75N92020D00004, N01-HC-95164, 75N92020D00007, N01-HC-95165, N01-HC-95166, N01-HC-95167, N01-HC-95168 and N01-HC-95169
Pays : United States
Organisme : NHLBI NIH HHS
ID : 75N92020D00001, HHSN268201500003I, N01-HC-95159, 75N92020D00005, N01-HC-95160, 75N92020D00002, N01-HC-95161, 75N92020D00003, N01-HC-95162, 75N92020D00006, N01-HC-95163, 75N92020D00004, N01-HC-95164, 75N92020D00007, N01-HC-95165, N01-HC-95166, N01-HC-95167, N01-HC-95168 and N01-HC-95169
Pays : United States
Organisme : NCATS NIH HHS
ID : UL1-TR-000040, UL1-TR-001079, and UL1-TR-001420
Pays : United States
Organisme : NCATS NIH HHS
ID : UL1-TR-000040, UL1-TR-001079, and UL1-TR-001420
Pays : United States
Informations de copyright
© 2024. The Author(s).
Références
Zhang, C., Rexrode, K. M., van Dam, R. M., Li, T. Y. & Hu, F. B. Abdominal obesity and the risk of all-cause, cardiovascular, and cancer mortality. Circulation 117(13), 1658–1667. https://doi.org/10.1161/CIRCULATIONAHA.107.739714 (2008).
doi: 10.1161/CIRCULATIONAHA.107.739714
pubmed: 18362231
Miljkovic, I., Vella, C. A. & Allison, M. Computed tomography-derived myosteatosis and metabolic disorders. Diabetes Metab. J. 45(4), 482–491. https://doi.org/10.4093/dmj.2020.0277 (2021).
doi: 10.4093/dmj.2020.0277
pubmed: 34352985
pmcid: 8369205
De Marco, D. et al. Muscle area and density assessed by abdominal computed tomography in healthy adults: Effect of normal aging and derivation of reference values. J. Nutr. Health Aging 26(2), 243–246. https://doi.org/10.1007/s12603-022-1746-3 (2022).
doi: 10.1007/s12603-022-1746-3
pubmed: 35297466
Singh, R., Artaza, J. N., Taylor, W. E., Gonzalez-Cadavid, N. F. & Bhasin, S. Androgens stimulate myogenic differentiation and inhibit adipogenesis in C3H 10T1/2 pluripotent cells through an androgen receptor-mediated pathway. Endocrinology 144(11), 5081–5088. https://doi.org/10.1210/en.2003-0741 (2003).
doi: 10.1210/en.2003-0741
pubmed: 12960001
Sinha-Hikim, I. et al. Testosterone-induced increase in muscle size in healthy young men is associated with muscle fiber hypertrophy. Am. J. Physiol. Endocrinol. Metab. 283(1), E154–E164. https://doi.org/10.1152/ajpendo.00502.2001 (2002).
doi: 10.1152/ajpendo.00502.2001
pubmed: 12067856
Kelly, D. M. & Jones, T. H. Testosterone: A metabolic hormone in health and disease. J. Endocrinol. 217(3), R25-45. https://doi.org/10.1530/joe-12-0455 (2013).
doi: 10.1530/joe-12-0455
pubmed: 23378050
Srinivas-Shankar, U. et al. Effects of testosterone on muscle strength, physical function, body composition, and quality of life in intermediate-frail and frail elderly men: A randomized, double-blind, placebo-controlled study. J. Clin. Endocrinol. Metab. 95(2), 639–650. https://doi.org/10.1210/jc.2009-1251 (2010).
doi: 10.1210/jc.2009-1251
pubmed: 20061435
Russell, N. & Grossmann, M. MECHANISMS IN ENDOCRINOLOGY: Estradiol as a male hormone. Eur. J. Endocrinol. 181(1), R23–R43. https://doi.org/10.1530/eje-18-1000 (2019).
doi: 10.1530/eje-18-1000
pubmed: 31096185
Vandenput, L. et al. Serum estradiol is associated with lean mass in elderly Swedish men. Eur. J. Endocrinol. 162(4), 737–745. https://doi.org/10.1530/eje-09-0696 (2010).
doi: 10.1530/eje-09-0696
pubmed: 20061331
Finkelstein, J. S. et al. Gonadal steroids and body composition, strength, and sexual function in men. N. Engl. J. Med. 369(11), 1011–1022. https://doi.org/10.1056/NEJMoa1206168 (2013).
doi: 10.1056/NEJMoa1206168
pubmed: 24024838
pmcid: 4142768
Baracos, V. E. Psoas as a sentinel muscle for sarcopenia: A flawed premise. J Cachexia Sarcopenia Muscle. 8(4), 527–528. https://doi.org/10.1002/jcsm.12221 (2017).
doi: 10.1002/jcsm.12221
pubmed: 28675689
pmcid: 5566635
Häggmark, T. & Thorstensson, A. Fibre types in human abdominal muscles. Acta Physiol. Scand. 107(4), 319–325. https://doi.org/10.1111/j.1748-1716.1979.tb06482.x (1979).
doi: 10.1111/j.1748-1716.1979.tb06482.x
pubmed: 161688
Goodpaster, B. H. et al. Attenuation of skeletal muscle and strength in the elderly: The Health ABC Study. J. Appl. Physiol. (1985) 90(6), 2157–2165. https://doi.org/10.1152/jappl.2001.90.6.2157 (2001).
doi: 10.1152/jappl.2001.90.6.2157
pubmed: 11356778
He, J., Watkins, S. & Kelley, D. E. Skeletal muscle lipid content and oxidative enzyme activity in relation to muscle fiber type in type 2 diabetes and obesity. Diabetes 50(4), 817–823. https://doi.org/10.2337/diabetes.50.4.817 (2001).
doi: 10.2337/diabetes.50.4.817
pubmed: 11289047
Herbst, K. L. & Bhasin, S. Testosterone action on skeletal muscle. Curr. Opin. Clin. Nutr. Metab. Care 7(3), 271–277. https://doi.org/10.1097/00075197-200405000-00006 (2004).
doi: 10.1097/00075197-200405000-00006
pubmed: 15075918
Woodhouse, L. J. et al. Dose-dependent effects of testosterone on regional adipose tissue distribution in healthy young men. J. Clin. Endocrinol. Metab. 89(2), 718–726. https://doi.org/10.1210/jc.2003-031492 (2004).
doi: 10.1210/jc.2003-031492
pubmed: 14764787
Han, S. et al. Testosterone is associated with abdominal body composition derived from computed tomography: A large cross sectional study. Sci. Rep. 12(1), 22528. https://doi.org/10.1038/s41598-022-27182-y (2022).
doi: 10.1038/s41598-022-27182-y
pubmed: 36581676
pmcid: 9800400
Hammes, A. et al. Role of endocytosis in cellular uptake of sex steroids. Cell 122(5), 751–762. https://doi.org/10.1016/j.cell.2005.06.032 (2005).
doi: 10.1016/j.cell.2005.06.032
pubmed: 16143106
Poole, C. N., Roberts, M. D., Dalbo, V. J., Sunderland, K. L. & Kerksick, C. M. Megalin and androgen receptor gene expression in young and old human skeletal muscle before and after three sequential exercise bouts. J. Strength Condition. Res. 25(2), 309–317. https://doi.org/10.1519/JSC.0b013e318202e45d (2011).
doi: 10.1519/JSC.0b013e318202e45d
Matsumine, H., Hirato, K., Yanaihara, T., Tamada, T. & Yoshida, M. Aromatization by skeletal muscle. J. Clin. Endocrinol. Metab. 63(3), 717–720. https://doi.org/10.1210/jcem-63-3-717 (1986).
doi: 10.1210/jcem-63-3-717
pubmed: 3734038
Barros Rodrigo, P. A. & Gustafsson, J. -Å. Estrogen receptors and the metabolic network. Cell Metab. 14(3), 289–299. https://doi.org/10.1016/j.cmet.2011.08.005 (2011).
doi: 10.1016/j.cmet.2011.08.005
pubmed: 21907136
Velez, L. M. et al. Genetic variation of putative myokine signaling is dominated by biological sex and sex hormones. Elife 11, e76887. https://doi.org/10.7554/eLife.76887 (2022).
doi: 10.7554/eLife.76887
pubmed: 35416774
pmcid: 9094747
Wiik, A. et al. Expression of oestrogen receptor alpha and beta is higher in skeletal muscle of highly endurance-trained than of moderately active men. Acta Physiol. Scand. 184(2), 105–112. https://doi.org/10.1111/j.1365-201X.2005.01433.x (2005).
doi: 10.1111/j.1365-201X.2005.01433.x
pubmed: 15916670
Maher, A. C., Akhtar, M. & Tarnopolsky, M. A. Men supplemented with 17beta-estradiol have increased beta-oxidation capacity in skeletal muscle. Physiol Genomics 42(3), 342–347. https://doi.org/10.1152/physiolgenomics.00016.2010 (2010).
doi: 10.1152/physiolgenomics.00016.2010
pubmed: 20484157
Svensson, J., Movérare-Skrtic, S., Windahl, S., Swanson, C. & Sjögren, K. Stimulation of both estrogen and androgen receptors maintains skeletal muscle mass in gonadectomized male mice but mainly via different pathways. J. Mol. Endocrinol. 45(1), 45–57. https://doi.org/10.1677/jme-09-0165 (2010).
doi: 10.1677/jme-09-0165
pubmed: 20435684
Wang, Q. et al. Sex hormone-binding globulin associations with circulating lipids and metabolites and the risk for type 2 diabetes: Observational and causal effect estimates. Int. J. Epidemiol. 44(2), 623–637. https://doi.org/10.1093/ije/dyv093 (2015).
doi: 10.1093/ije/dyv093
pubmed: 26050255
Osmancevic, A., Daka, B., Michos, E. D., Trimpou, P. & Allison, M. The association between inflammation, testosterone and SHBG in men: A cross-sectional Multi-Ethnic Study of Atherosclerosis. Clin. Endocrinol. (Oxf.) https://doi.org/10.1111/cen.14930 (2023).
doi: 10.1111/cen.14930
pubmed: 37221937
Yuki, A. et al. Relationship between low free testosterone levels and loss of muscle mass. Sci. Rep. 3(1), 1818. https://doi.org/10.1038/srep01818 (2013).
doi: 10.1038/srep01818
pubmed: 23660939
pmcid: 6504823
Auyeung, T. W. et al. Testosterone but not estradiol level is positively related to muscle strength and physical performance independent of muscle mass: A cross-sectional study in 1489 older men. Eur. J. Endocrinol. 164(5), 811–817. https://doi.org/10.1530/eje-10-0952 (2011).
doi: 10.1530/eje-10-0952
pubmed: 21346095
Narinx, N. et al. Role of sex hormone-binding globulin in the free hormone hypothesis and the relevance of free testosterone in androgen physiology. Cell Mol. Life Sci. 79(11), 543. https://doi.org/10.1007/s00018-022-04562-1 (2022).
doi: 10.1007/s00018-022-04562-1
pubmed: 36205798
Larsen, B. et al. Muscle area and density and risk of all-cause mortality: The Multi-Ethnic Study of Atherosclerosis. Metabolism 111, 154321. https://doi.org/10.1016/j.metabol.2020.154321 (2020).
doi: 10.1016/j.metabol.2020.154321
pubmed: 32712219
pmcid: 8062068
Al-Sharefi, A. & Quinton, R. Current national and international guidelines for the management of male hypogonadism: Helping clinicians to navigate variation in diagnostic criteria and treatment recommendations. Endocrinol. Metab. (Seoul) 35(3), 526–540. https://doi.org/10.3803/EnM.2020.760 (2020).
doi: 10.3803/EnM.2020.760
pubmed: 32981295
Schweitzer, L. et al. What is the best reference site for a single MRI slice to assess whole-body skeletal muscle and adipose tissue volumes in healthy adults?. Am. J. Clin. Nutr. 102(1), 58–65. https://doi.org/10.3945/ajcn.115.111203 (2015).
doi: 10.3945/ajcn.115.111203
pubmed: 26016860
Trost, L. W. & Mulhall, J. P. Challenges in testosterone measurement, data interpretation, and methodological appraisal of interventional trials. J. Sex Med. 13(7), 1029–1046. https://doi.org/10.1016/j.jsxm.2016.04.068 (2016).
doi: 10.1016/j.jsxm.2016.04.068
pubmed: 27209182
pmcid: 5516925
Wang, C., Catlin, D. H., Demers, L. M., Starcevic, B. & Swerdloff, R. S. Measurement of total serum testosterone in adult men: Comparison of current laboratory methods versus liquid chromatography-tandem mass spectrometry. J. Clin. Endocrinol. Metab. 89(2), 534–543. https://doi.org/10.1210/jc.2003-031287 (2004).
doi: 10.1210/jc.2003-031287
pubmed: 14764758
Krasowski, M. D. et al. Cross-reactivity of steroid hormone immunoassays: Clinical significance and two-dimensional molecular similarity prediction. BMC Clin. Pathol. 14, 33. https://doi.org/10.1186/1472-6890-14-33 (2014).
doi: 10.1186/1472-6890-14-33
pubmed: 25071417
pmcid: 4112981
Ly, L. P. & Handelsman, D. J. Empirical estimation of free testosterone from testosterone and sex hormone-binding globulin immunoassays. Eur. J. Endocrinol. 152(3), 471–478. https://doi.org/10.1530/eje.1.01844 (2005).
doi: 10.1530/eje.1.01844
pubmed: 15757865
Vermeulen, A., Verdonck, L. & Kaufman, J. M. A critical evaluation of simple methods for the estimation of free testosterone in serum. J. Clin. Endocrinol. Metab. 84(10), 3666–3672. https://doi.org/10.1210/jcem.84.10.6079 (1999).
doi: 10.1210/jcem.84.10.6079
pubmed: 10523012
de Ronde, W. et al. Calculation of bioavailable and free testosterone in men: A comparison of 5 published algorithms. Clin Chem. 52(9), 1777–1784. https://doi.org/10.1373/clinchem.2005.063354 (2006).
doi: 10.1373/clinchem.2005.063354
pubmed: 16793931
Bild, D. E. et al. Multi-Ethnic Study of atherosclerosis: Objectives and design. Am. J. Epidemiol. 156(9), 871–881. https://doi.org/10.1093/aje/kwf113 (2002).
doi: 10.1093/aje/kwf113
pubmed: 12397006
Bhatraju, P. K., Zelnick, L. R., Shlipak, M., Katz, R. & Kestenbaum, B. Association of soluble TNFR-1 concentrations with long-term decline in kidney function: The Multi-Ethnic Study of atherosclerosis. J. Am. Soc. Nephrol. 29(11), 2713–2721. https://doi.org/10.1681/asn.2018070719 (2018).
doi: 10.1681/asn.2018070719
pubmed: 30287518
pmcid: 6218870
Ainsworth, B. E., Irwin, M. L., Addy, C. L., Whitt, M. C. & Stolarczyk, L. M. Moderate physical activity patterns of minority women: The Cross-Cultural Activity Participation Study. J. Womens Health Gend Based Med. 8(6), 805–813. https://doi.org/10.1089/152460999319129 (1999).
doi: 10.1089/152460999319129
pubmed: 10495261
Psaty, B. M. et al. Assessing the use of medications in the elderly: Methods and initial experience in the Cardiovascular Health Study. The Cardiovascular Health Study Collaborative Research Group. J. Clin. Epidemiol. 45(6), 683–692. https://doi.org/10.1016/0895-4356(92)90143-b (1992).
doi: 10.1016/0895-4356(92)90143-b
pubmed: 1607909
Kramer, H. et al. Racial/ethnic differences in hypertension and hypertension treatment and control in the Multi-Ethnic Study of atherosclerosis (MESA). Am. J. Hypertens. 17(10), 963–970. https://doi.org/10.1016/j.amjhyper.2004.06.001 (2004).
doi: 10.1016/j.amjhyper.2004.06.001
pubmed: 15485761
Bertoni, A. G., Kramer, H., Watson, K. & Post, W. S. Diabetes and clinical and subclinical CVD. Glob Heart. 11(3), 337–342. https://doi.org/10.1016/j.gheart.2016.07.005 (2016).
doi: 10.1016/j.gheart.2016.07.005
pubmed: 27741980
Harhay, M. O. et al. Relationship of CRP, IL-6, and fibrinogen with right ventricular structure and function: The MESA-Right Ventricle Study. Int. J. Cardiol. 168(4), 3818–3824. https://doi.org/10.1016/j.ijcard.2013.06.028 (2013).
doi: 10.1016/j.ijcard.2013.06.028
pubmed: 23932860
pmcid: 3805818
Aubrey, J. et al. Measurement of skeletal muscle radiation attenuation and basis of its biological variation. Acta Physiol. (Oxf.) 210(3), 489–497. https://doi.org/10.1111/apha.12224 (2014).
doi: 10.1111/apha.12224
pubmed: 24393306
Goodpaster, B. H., Thaete, F. L. & Kelley, D. E. Composition of skeletal muscle evaluated with computed tomography. Ann. N. Y. Acad. Sci. 904, 18–24. https://doi.org/10.1111/j.1749-6632.2000.tb06416.x (2000).
doi: 10.1111/j.1749-6632.2000.tb06416.x
pubmed: 10865705
Zhao, D. et al. Endogenous sex hormones and incident cardiovascular disease in post-menopausal women. J. Am. Coll. Cardiol. 71(22), 2555–2566. https://doi.org/10.1016/j.jacc.2018.01.083 (2018).
doi: 10.1016/j.jacc.2018.01.083
pubmed: 29852978
pmcid: 5986086
Michos, E. D. et al. Sex hormones, sex hormone binding globulin, and abdominal aortic calcification in women and men in the Multi-Ethnic Study of atherosclerosis (MESA). Atherosclerosis. 200(2), 432–438. https://doi.org/10.1016/j.atherosclerosis.2007.12.032 (2008).
doi: 10.1016/j.atherosclerosis.2007.12.032
pubmed: 18262187
pmcid: 2607033
Golden, S. H. et al. Endogenous sex hormones and glucose tolerance status in postmenopausal women. J. Clin. Endocrinol. Metab. 92(4), 1289–1295. https://doi.org/10.1210/jc.2006-1895 (2007).
doi: 10.1210/jc.2006-1895
pubmed: 17244779
Södergård, R., Bäckström, T., Shanbhag, V. & Carstensen, H. Calculation of free and bound fractions of testosterone and estradiol-17 beta to human plasma proteins at body temperature. J. Steroid. Biochem. 16(6), 801–810. https://doi.org/10.1016/0022-4731(82)90038-3 (1982).
doi: 10.1016/0022-4731(82)90038-3
pubmed: 7202083