Endocrinol Metab.  2019 Jun;34(2):158-168. 10.3803/EnM.2019.34.2.158.

Associations of Metabolic Syndrome with Total Testosterone and Homocysteine Levels in Male Korean Workers

Affiliations
  • 1Radiation Health Institute, Korea Hydro and Nuclear Power Co., Ltd., Seongnam, Korea. sjchoice@naver.com

Abstract

BACKGROUND
Low testosterone is associated with metabolic syndrome (MetS), and homocysteine (Hcy) is elevated in individuals with MetS. We investigated the relationships of total testosterone (TT) and serum Hcy levels with MetS in male Korean workers.
METHODS
We conducted a cross-sectional study including 8,606 male workers, aged 20 to 58 years, who underwent a physical examination in 2015. MetS was diagnosed based on the criteria of the 2009 harmonized definition, while the Korean standard for waist circumference (WC) was used. Participants' biochemical parameters, including TT and serum Hcy, were measured, and participants were divided into quartiles. Multiple logistic regression models were used to estimate the association of MetS and its individual components depending on TT and serum Hcy quartiles.
RESULTS
The prevalence of MetS in the study population was 16%. TT was lower in participants with MetS than in those without MetS (P<0.001). By contrast, Hcy level was similar between groups (P=0.694). In multiple logistic regression analysis, the odds ratio for the lowest TT quartile was 1.29 (95% confidence interval, 1.06 to 1.57) after adjusting for potential confounders. Participants with lower TT were more likely to have high WC, hypertriglyceridemia, and low high density lipoprotein levels. Serum Hcy levels were not significantly associated with MetS. Of the five components of MetS, only WC was significantly associated with serum Hcy.
CONCLUSION
In male Korean workers, TT may be an independent predictor of MetS, and serum Hcy levels could be a marker of abdominal obesity. However, future prospective studies are needed.

Keyword

Testosterone; Homocysteine; Metabolic syndrome; Odds ratio

MeSH Terms

Cross-Sectional Studies
Homocysteine*
Humans
Hypertriglyceridemia
Lipoproteins
Logistic Models
Male*
Obesity, Abdominal
Odds Ratio
Physical Examination
Prevalence
Prospective Studies
Testosterone*
Waist Circumference
Homocysteine
Lipoproteins
Testosterone

Figure

  • Fig. 1 Distribution of the prevalence of metabolic syndrome (MetS) and the number of MetS components depending on total testosterone (TT) and serum homocysteine (Hcy) quartiles in 8,606 male workers. (A) The number of MetS components was significantly different from the first (Q1) to the fourth (Q4) TT quartiles (P<0.001). However, the number of MetS components was not related to serum Hcy quartile (P=0.361). (B) The prevalence of MetS showed similar relationships with TT and serum Hcy quartiles (P<0.001 and P=0.361, respectively).


Reference

1. Lim S, Shin H, Song JH, Kwak SH, Kang SM, Won Yoon J, et al. Increasing prevalence of metabolic syndrome in Korea: the Korean National Health and Nutrition Examination Survey for 1998-2007. Diabetes Care. 2011; 34:1323–1328. PMID: 21505206.
2. Andreadis EA, Tsourous GI, Tzavara CK, Georgiopoulos DX, Katsanou PM, Marakomichelakis GE, et al. Metabolic syndrome and incident cardiovascular morbidity and mortality in a Mediterranean hypertensive population. Am J Hypertens. 2007; 20:558–564. PMID: 17485022.
Article
3. Brand JS, Rovers MM, Yeap BB, Schneider HJ, Tuomainen TP, Haring R, et al. Testosterone, sex hormone-binding globulin and the metabolic syndrome in men: an individual participant data meta-analysis of observational studies. PLoS One. 2014; 9:e100409. PMID: 25019163.
Article
4. Haring R, Volzke H, Felix SB, Schipf S, Dorr M, Rosskopf D, et al. Prediction of metabolic syndrome by low serum testosterone levels in men: results from the study of health in Pomerania. Diabetes. 2009; 58:2027–2031. PMID: 19581420.
5. Li C, Ford ES, Li B, Giles WH, Liu S. Association of testosterone and sex hormone-binding globulin with metabolic syndrome and insulin resistance in men. Diabetes Care. 2010; 33:1618–1624. PMID: 20368409.
Article
6. Kupelian V, Page ST, Araujo AB, Travison TG, Bremner WJ, McKinlay JB. Low sex hormone-binding globulin, total testosterone, and symptomatic androgen deficiency are associated with development of the metabolic syndrome in nonobese men. J Clin Endocrinol Metab. 2006; 91:843–850. PMID: 16394089.
Article
7. Laaksonen DE, Niskanen L, Punnonen K, Nyyssonen K, Tuomainen TP, Valkonen VP, et al. Testosterone and sex hormone-binding globulin predict the metabolic syndrome and diabetes in middle-aged men. Diabetes Care. 2004; 27:1036–1041. PMID: 15111517.
Article
8. Yeap BB, Chubb SA, Hyde Z, Jamrozik K, Hankey GJ, Flicker L, et al. Lower serum testosterone is independently associated with insulin resistance in non-diabetic older men: the Health In Men Study. Eur J Endocrinol. 2009; 161:591–598. PMID: 19661128.
Article
9. Tsai EC, Boyko EJ, Leonetti DL, Fujimoto WY. Low serum testosterone level as a predictor of increased visceral fat in Japanese-American men. Int J Obes Relat Metab Disord. 2000; 24:485–491. PMID: 10805506.
Article
10. Rao PM, Kelly DM, Jones TH. Testosterone and insulin resistance in the metabolic syndrome and T2DM in men. Nat Rev Endocrinol. 2013; 9:479–493. PMID: 23797822.
Article
11. Fonseca V, Guba SC, Fink LM. Hyperhomocysteinemia and the endocrine system: implications for atherosclerosis and thrombosis. Endocr Rev. 1999; 20:738–759. PMID: 10529901.
Article
12. Wald DS, Law M, Morris JK. Homocysteine and cardiovascular disease: evidence on causality from a meta-analysis. BMJ. 2002; 325:1202. PMID: 12446535.
Article
13. Meigs JB, Jacques PF, Selhub J, Singer DE, Nathan DM, Rifai N, et al. Fasting plasma homocysteine levels in the insulin resistance syndrome: the Framingham offspring study. Diabetes Care. 2001; 24:1403–1410. PMID: 11473077.
14. Wang X, Ye P, Cao R, Yang X, Xiao W, Zhang Y, et al. The association of homocysteine with metabolic syndrome in a community-dwelling population: homocysteine might be concomitant with metabolic syndrome. PLoS One. 2014; 9:e113148. PMID: 25401978.
Article
15. Alberti KG, Eckel RH, Grundy SM, Zimmet PZ, Cleeman JI, Donato KA, et al. Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation. 2009; 120:1640–1645. PMID: 19805654.
16. Lee SY, Park HS, Kim DJ, Han JH, Kim SM, Cho GJ, et al. Appropriate waist circumference cutoff points for central obesity in Korean adults. Diabetes Res Clin Pract. 2007; 75:72–80. PMID: 16735075.
Article
17. Muller M, Grobbee DE, den Tonkelaar I, Lamberts SW, van der Schouw YT. Endogenous sex hormones and metabolic syndrome in aging men. J Clin Endocrinol Metab. 2005; 90:2618–2623. PMID: 15687322.
Article
18. Hong D, Kim YS, Son ES, Kim KN, Kim BT, Lee DJ, et al. Total testosterone and sex hormone-binding globulin are associated with metabolic syndrome independent of age and body mass index in Korean men. Maturitas. 2013; 74:148–153. PMID: 23218685.
Article
19. Cohen PG. The hypogonadal-obesity cycle: role of aromatase in modulating the testosterone-estradiol shunt: a major factor in the genesis of morbid obesity. Med Hypotheses. 1999; 52:49–51. PMID: 10342671.
20. Chatterjee C, Sparks DL. Hepatic lipase, high density lipoproteins, and hypertriglyceridemia. Am J Pathol. 2011; 178:1429–1433. PMID: 21406176.
Article
21. Thuren T. Hepatic lipase and HDL metabolism. Curr Opin Lipidol. 2000; 11:277–283. PMID: 10882343.
Article
22. Van Pottelbergh I, Braeckman L, De Bacquer D, De Backer G, Kaufman JM. Differential contribution of testosterone and estradiol in the determination of cholesterol and lipoprotein profile in healthy middle-aged men. Atherosclerosis. 2003; 166:95–102. PMID: 12482555.
Article
23. Stanworth RD, Kapoor D, Channer KS, Jones TH. Dyslipidaemia is associated with testosterone, oestradiol and androgen receptor CAG repeat polymorphism in men with type 2 diabetes. Clin Endocrinol (Oxf). 2011; 74:624–630. PMID: 21470285.
Article
24. Kupelian V, Hayes FJ, Link CL, Rosen R, McKinlay JB. Inverse association of testosterone and the metabolic syndrome in men is consistent across race and ethnic groups. J Clin Endocrinol Metab. 2008; 93:3403–3410. PMID: 18559915.
Article
25. Akishita M, Fukai S, Hashimoto M, Kameyama Y, Nomura K, Nakamura T, et al. Association of low testosterone with metabolic syndrome and its components in middle-aged Japanese men. Hypertens Res. 2010; 33:587–591. PMID: 20339372.
Article
26. Litman HJ, Bhasin S, Link CL, Araujo AB, McKinlay JB. Serum androgen levels in black, Hispanic, and white men. J Clin Endocrinol Metab. 2006; 91:4326–4334. PMID: 16912139.
Article
27. Orwoll E, Lambert LC, Marshall LM, Phipps K, Blank J, Barrett-Connor E, et al. Testosterone and estradiol among older men. J Clin Endocrinol Metab. 2006; 91:1336–1344. PMID: 16368750.
Article
28. Catena C, Colussi G, Nait F, Capobianco F, Sechi LA. Elevated homocysteine levels are associated with the metabolic syndrome and cardiovascular events in hypertensive patients. Am J Hypertens. 2015; 28:943–950. PMID: 25498997.
Article
29. Sreckovic B, Sreckovic VD, Soldatovic I, Colak E, Sumarac-Dumanovic M, Janeski H, et al. Homocysteine is a marker for metabolic syndrome and atherosclerosis. Diabetes Metab Syndr. 2017; 11:179–182. PMID: 27600468.
Article
30. Buysschaert M, Dramais AS, Wallemacq PE, Hermans MP. Hyperhomocysteinemia in type 2 diabetes: relationship to macroangiopathy, nephropathy, and insulin resistance. Diabetes Care. 2000; 23:1816–1822. PMID: 11128359.
Article
31. Nabipour I, Ebrahimi A, Jafari SM, Vahdat K, Assadi M, Movahed A, et al. The metabolic syndrome is not associated with homocysteinemia: the Persian Gulf Healthy Heart Study. J Endocrinol Invest. 2009; 32:406–410. PMID: 19794288.
Article
32. Tanrikulu-Kilic F, Bekpinar S, Unlucerci Y, Orhan Y. Insulin resistance is not related to plasma homocysteine concentration in healthy premenapausal women. Physiol Res. 2006; 55:285–290. PMID: 16083308.
33. Ganji V, Kafai MR. Third National Health and Nutrition Examination Survey. Demographic, health, lifestyle, and blood vitamin determinants of serum total homocysteine concentrations in the third National Health and Nutrition Examination Survey, 1988-1994. Am J Clin Nutr. 2003; 77:826–833. PMID: 12663279.
Article
34. McAndrew PE, Brandt JT, Pearl DK, Prior TW. The incidence of the gene for thermolabile methylene tetrahydrofolate reductase in African Americans. Thromb Res. 1996; 83:195–198. PMID: 8837319.
Article
35. Senaratne MP, MacDonald K, De Silva D. Possible ethnic differences in plasma homocysteine levels associated with coronary artery disease between south Asian and east Asian immigrants. Clin Cardiol. 2001; 24:730–734. PMID: 11714131.
Article
36. Anand SS, Yusuf S, Vuksan V, Devanesen S, Teo KK, Montague PA, et al. Differences in risk factors, atherosclerosis and cardiovascular disease between ethnic groups in Canada: the study of health assessment and risk in ethnic groups (SHARE). Indian Heart J. 2000; 52:S35–S43. PMID: 11339439.
Article
37. Cappuccio FP, Bell R, Perry IJ, Gilg J, Ueland PM, Refsum H, et al. Homocysteine levels in men and women of different ethnic and cultural background living in England. Atherosclerosis. 2002; 164:95–102. PMID: 12119198.
Article
38. Esteghamati A, Hafezi-Nejad N, Zandieh A, Sheikhbahaei S, Ebadi M, Nakhjavani M. Homocysteine and metabolic syndrome: from clustering to additional utility in prediction of coronary heart disease. J Cardiol. 2014; 64:290–296. PMID: 24631466.
Article
39. Rhee EJ, Hwang ST, Lee WY, Yoon JH, Kim BJ, Kim BS, et al. Relationship between metabolic syndrome categorized by newly recommended by International Diabetes Federation criteria with plasma homocysteine concentration. Endocr J. 2007; 54:995–1002. PMID: 18079590.
Article
40. Shin KA. Association between obesity factors and homocysteine levels with the metabolic syndrome. Korean J Clin Lab Sci. 2012; 44:147–154.
41. Vaya A, Rivera L, Hernandez-Mijares A, de la Fuente M, Sola E, Romagnoli M, et al. Homocysteine levels in morbidly obese patients: its association with waist circumference and insulin resistance. Clin Hemorheol Microcirc. 2012; 52:49–56. PMID: 22460264.
42. Park SB, Georgiades A. Changes in body composition predict homocysteine changes and hyperhomocysteinemia in Korea. J Korean Med Sci. 2013; 28:1015–1020. PMID: 23853483.
Article
43. Abbasi F, Facchini F, Humphreys MH, Reaven GM. Plasma homocysteine concentrations in healthy volunteers are not related to differences in insulin-mediated glucose disposal. Atherosclerosis. 1999; 146:175–178. PMID: 10487501.
Article
44. Godsland IF, Rosankiewicz JR, Proudler AJ, Johnston DG. Plasma total homocysteine concentrations are unrelated to insulin sensitivity and components of the metabolic syndrome in healthy men. J Clin Endocrinol Metab. 2001; 86:719–723. PMID: 11158036.
Article
45. Nakazato M, Maeda T, Takamura N, Wada M, Yamasaki H, Johnston KE, et al. Relation of body mass index to blood folate and total homocysteine concentrations in Japanese adults. Eur J Nutr. 2011; 50:581–585. PMID: 21221977.
Article
46. Mojtabai R. Body mass index and serum folate in childbearing age women. Eur J Epidemiol. 2004; 19:1029–1036. PMID: 15648596.
Article
47. Bravo E, Palleschi S, Aspichueta P, Buque X, Rossi B, Cano A, et al. High fat diet-induced non alcoholic fatty liver disease in rats is associated with hyperhomocysteinemia caused by down regulation of the transsulphuration pathway. Lipids Health Dis. 2011; 10:60. PMID: 21504583.
Article
48. Fonseca VA, Mudaliar S, Schmidt B, Fink LM, Kern PA, Henry RR. Plasma homocysteine concentrations are regulated by acute hyperinsulinemia in nondiabetic but not type 2 diabetic subjects. Metabolism. 1998; 47:686–689. PMID: 9627367.
Article
49. Rosolova H, Simon J, Mayer O Jr, Racek J, Dierze T, Jacobsen DW. Unexpected inverse relationship between insulin resistance and serum homocysteine in healthy subjects. Physiol Res. 2002; 51:93–98. PMID: 12071296.
50. Pitsavos C, Panagiotakos D, Weinem M, Stefanadis C. Diet, exercise and the metabolic syndrome. Rev Diabet Stud. 2006; 3:118–126. PMID: 17487335.
Article
Full Text Links
  • ENM
Actions
Cited
CITED
export Copy
Close
Share
  • Twitter
  • Facebook
Similar articles
Copyright © 2024 by Korean Association of Medical Journal Editors. All rights reserved.     E-mail: koreamed@kamje.or.kr