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Changes in Sex Hormones After Laparoscopic Sleeve Gastrectomy in Chinese Obese Men: a 12-Month Follow-Up

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Abstract

Background

To examine changes in sex hormones after laparoscopic sleeve gastrectomy (LSG) in Chinese obese male patients and their correlation with metabolic parameters including serum uric acid (SUA)

Methods

A total of 56 obese men with body mass index (BMI) 41.9 ± 5.8 kg/m2 undergoing LSG were selected. Thirty-one healthy men with normal BMI were included as controls. Levels of total testosterone (TT), estradiol (E2), sex hormone-binding globulin (SHBG), follicle-stimulating hormone (FSH), luteinizing hormone (LH), SUA, and other metabolic indices were compared pre- and 12 months post-LSG. Calculated free testosterone (cFT) was calculated from TT and SHBG using an empirical equation.

Results

At baseline, low TT and hyperuricemia (HUA) were common in obese men. Twelve months after LSG, statistically significant reduction in weight, BMI, and glucolipid metabolism indices was noted. SUA levels declined remarkably from 474.9 ± 94.6 to 338.8 ± 81.9 μmol/L and the percentage of HUA decreased from 76.8 to 54.1% (all P < 0.001). Additionally, significant increases in TT, SHBG, and cFT as well as a decrease in percentage of low TT were observed after LSG (all P < 0.05), while E2, FSH, and LH did not change significantly. Moreover, changes in TT levels were more pronounced than those of other sex hormones. After age and BMI were adjusted, increased TT levels were correlated significantly with decreased SUA (β = − 1.077, P < 0.05), BMI (β = − 0.712, P < 0.001), and HOMA-IR (β = − 0.652, P < 0.05), as well as increased SHBG (β = 0.759, P < 0.001).

Conclusions

LSG promotes a significant increase in TT levels in Chinese obese men, which may be mediated by substantial weight loss, SUA reduction, and improved insulin resistance (IR).

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References

  1. Ng M, Fleming T, Robinson M, et al. Global, regional, and national prevalence of overweight and obesity in children and adults during 1980-2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet. 2014;384(9945):766–81.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Kelly DM, Jones TH. Testosterone and obesity. Obes Rev. 2015;16(7):581–606.

    Article  CAS  PubMed  Google Scholar 

  3. Hofstra J, Loves S, van Wageningen B, et al. High prevalence of hypogonadotropic hypogonadism in men referred for obesity treatment. Neth J Med. 2008;66(3):103–9.

    CAS  PubMed  Google Scholar 

  4. Tanabe M, Akehi Y, Nomiyama T, et al. Total testosterone is the most valuable indicator of metabolic syndrome among various testosterone values in middle-aged Japanese men. Endocr J. 2015;62(2):123–32.

    Article  CAS  PubMed  Google Scholar 

  5. Grossmann M. Low testosterone in men with type 2 diabetes: significance and treatment. J Clin Endocrinol Metab. 2011;96(8):2341–53.

    Article  CAS  PubMed  Google Scholar 

  6. Naifar M, Rekik N, Messedi M, et al. Male hypogonadism and metabolic syndrome. Andrologia. 2015;47(5):579–86.

    Article  CAS  PubMed  Google Scholar 

  7. Osuna JA, Gómez-Pérez R, Arata-Bellabarba G, et al. Relationship between BMI, total testosterone, sex hormone-binding-globulin, leptin, insulin and insulin resistance in obese men. Arch Androl. 2006;52(5):355-61. 

  8. Zitzmann M. Testosterone deficiency, insulin resistance and the metabolic syndrome. Nat Rev Endocrinol. 2009;5(12):673-81. 

  9. Kivity S, Kopel E, Maor E, et al. Association of serum uric acid and cardiovascular disease in healthy adults. Am J Cardiol. 2013;111(8):1146–51.

    Article  CAS  PubMed  Google Scholar 

  10. Grayson PC, Kim SY, LaValley M, Choi HK. Hyperuricemia and incident hypertension: A systematic review and meta‐analysis. Arthritis Care Res. 2011;63(1):102–10.

  11. Li Q, Yang Z, Lu B, et al. Serum uric acid level and its association with metabolic syndrome and carotid atherosclerosis in patients with type 2 diabetes. Cardiovasc Diabetol. 2011;10(1):72.

  12. Cao W, Zheng RD, Xu SH, et al. Association between sex hormone and blood uric acid in male patients with type 2 diabetes. Int J Endocrinol. 2017;2017:4375253.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Hurina NM, Korpacheva-Zinych OV, Shuprovych AA. Interrelations of uric acid metabolism indices with insulin and testosterone levels in men with type 2 diabetes. Fiziolohichny Zhurnal. 2010;56(6):93–9.

    CAS  Google Scholar 

  14. Paulus GF, de Vaan LE, Verdam FJ, et al. Bariatric surgery in morbidly obese adolescents: a systematic review and meta-analysis. Obes Surg. 2015;25(5):860–78.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Inge TH, Courcoulas AP, Jenkins TM, et al. Weight loss and health status 3 years after bariatric surgery in adolescents. N Engl J Med. 2016;374(2):113–23.

    Article  CAS  PubMed  Google Scholar 

  16. Boonchaya-Anant P, Laichuthai N, Suwannasrisuk P, et al. Changes in testosterone levels and sex hormone-binding globulin levels in extremely obese men after bariatric surgery. Int J Endocrinol. 2016;2016(10):1416503.

    PubMed  PubMed Central  Google Scholar 

  17. Reis LO, Favaro WJ, Barreiro GC, et al. Erectile dysfunction and hormonal imbalance in morbidly obese male is reversed after gastric bypass surgery: a prospective randomized controlled trial. Int J Androl. 2010;33(5):736–44.

    Article  CAS  PubMed  Google Scholar 

  18. Gao J, Zhang M, Zhu C, et al. The change in the percent of android and gynoid fat mass correlated with increased testosterone after laparoscopic sleeve gastrectomy in Chinese obese men: a 6-month follow-up. Obes Surg. 2018;28(7):1960–5.

    Article  PubMed  Google Scholar 

  19. Oberbach A, Neuhaus J, Inge T, et al. Bariatric surgery in severely obese adolescents improves major comorbidities including hyperuricemia. Metabolism. 2014;63(2):242–9.

    Article  CAS  PubMed  Google Scholar 

  20. Sjostrom L, Lindroos AK, Peltonen M, et al. Lifestyle, diabetes, and cardiovascular risk factors 10 years after bariatric surgery. N Engl J Med. 2004;351:2683–93.

    Article  PubMed  Google Scholar 

  21. Richette P, Poitou C, Manivet P, et al. Weight loss, xanthine oxidase, and serum urate levels: a prospective longitudinal study of obese patients. Arthritis Care Res. 2016;68(7):1036–42.

    Article  CAS  Google Scholar 

  22. Dalbeth N, Chen P, White M, et al. Impact of bariatric surgery on serum urate targets in people with morbid obesity and diabetes: a prospective longitudinal study. Ann Rheum Dis. 2014;73:797–802.

    Article  CAS  PubMed  Google Scholar 

  23. Chen C, Lu FC, Department of Disease Control Ministry of Health PRC. The guidelines for prevention and control of overweight and obesity in Chinese adults. Biomed Environ Sci. 2004;17(Suppl):1–36.

    PubMed  Google Scholar 

  24. Jordan KM, Cameron JS, Snaith M, et al. British Society for Rheumatology and British health professionals in Rheumatology guideline for the management of gout. Rheumatology (Oxford). 2007;46(8):1372–4.

    Article  Google Scholar 

  25. van de Laar A, de Caluwe L, Dillemans B. Relative outcome measures for bariatric surgery. Evidence against excess weight loss and excess body mass index loss from a series of laparoscopic Roux-en-Y gastric bypass patients. Obes Surg. 2011;21(6):763–7.

    Article  PubMed  Google Scholar 

  26. Sartorius G, Ly LP, Sikaris K, et al. Predictive accuracy and sources of variability in calculated free testosterone estimates. Ann Clin Biochem. 2009;46(Pt 2):137–43.

    Article  CAS  PubMed  Google Scholar 

  27. Matthews DR, Hosker JP, Rudenski AS, et al. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985;28(7):412–9.

    Article  CAS  PubMed  Google Scholar 

  28. Khanna D, Fitzgerald JD, Khanna PP, et al. American College of Rheumatology guidelines for management of gout. Part 1: systematic nonpharmacologic and pharmacologic therapeutic approaches to hyperuricemia. Arthritis Care Res (Hoboken)2012. 2012;64(10):1431–46.

    Article  CAS  Google Scholar 

  29. Tajar A, Forti G, O'Neill TW, et al. Characteristics of secondary, primary, and compensated hypogonadism in aging men: evidence from the European Male Ageing Study. J Clin Endocrinol Metab. 2010;95(4):1810–8.

    Article  CAS  PubMed  Google Scholar 

  30. Civantos Modino S1, Guijarro de Armas MG, Monereo Mejías S, et al. Hyperuricemia and metabolic syndrome in children with overweight and obesity. Endocrinol Nutr. 2012;59(9):533-8.

  31. Mingrone G, Panunzi S, De Gaetano A, et al. Bariatric-metabolic surgery versus conventional medical treatment in obese patients with type 2 diabetes: 5 year follow-up of an open-label, single-centre, randomised controlled trial. Lancet. 2015;386(9997):964–73.

    Article  PubMed  Google Scholar 

  32. Remedios C, Shah M, Bhasker AG, et al. Hyperuricemia: a reality in the Indian obese. Obes Surg. 2012;22(6):945–8.

    Article  PubMed  Google Scholar 

  33. Luconi M, Samavat J, Seghieri G, et al. Determinants of testosterone recovery after bariatric surgery: is it only a matter of reduction of body mass index? Fertil Steril. 2013;99(7):1872–9.

    Article  CAS  PubMed  Google Scholar 

  34. Calderon B, Galdon A, Calanas A, et al. Effects of bariatric surgery on male obesity-associated secondary hypogonadism: comparison of laparoscopic gastric bypass with restrictive procedures. Obes Surg. 2014;24(10):1686–92.

    Article  PubMed  Google Scholar 

  35. Ricci C, Gaeta M, Rausa E, et al. Long-term effects of bariatric surgery on type II diabetes, hypertension and hyperlipidemia: a meta-analysis and meta-regression study with 5-year follow-up. Obes Surg. 2015;25(3):397–405.

    Article  PubMed  Google Scholar 

  36. Babio N, Martinez-Gonzalez MA, Estruch R, et al. Associations between serum uric acid concentrations and metabolic syndrome and its components in the PREDIMED study. Nutr Metab Cardiovasc Dis. 2015;25(2):173–80.

    Article  CAS  PubMed  Google Scholar 

  37. Serpa Neto A, Rossi FM, Valle LG, et al. Relation of uric acid with components of metabolic syndrome before and after Roux-en-Y gastric bypass in morbidly obese subjects. Arq Bras Endocrinol Metabol. 2011;55(1):38–45.

    Article  PubMed  Google Scholar 

  38. Wang W, Liou TH, Lee WJ, et al. ESR1 gene and insulin resistance remission are associated with serum uric acid decline for severely obese patients undergoing bariatric surgery. Surg Obes Relat Dis. 2014;10(1):14–22.

    Article  CAS  PubMed  Google Scholar 

  39. Pellitero S, Olaizola I, Alastrue A, et al. Hypogonadotropic hypogonadism in morbidly obese males is reversed after bariatric surgery. Obes Surg. 2012;22(12):1835–42.

    Article  PubMed  Google Scholar 

  40. Mihalca R, Copaescu C, Sirbu A, et al. Laparoscopic sleeve gastrectomy improves reproductive hormone levels in morbidly obese males—a series of 28 cases. Chirurgia. 2014;109(2):198–203.

    CAS  PubMed  Google Scholar 

  41. Botella-Carretero JI, Balsa JA, Gomez-Martin JM, et al. Circulating free testosterone in obese men after bariatric surgery increases in parallel with insulin sensitivity. J Endocrinol Investig. 2013;36(4):227–32.

    CAS  Google Scholar 

  42. Bastounis EA, Karayiannakis AJ, Syrigos K, et al. Sex hormone changes in morbidly obese patients after vertical banded gastroplasty. Eur Surg Res. 1998;30(1):43–7.

    Article  CAS  PubMed  Google Scholar 

  43. Caprio M, Fabbrini E, Isidori AM, et al. Leptin in reproduction. Trends Endocrinol Metab. 2001;12(2):65–72.

    Article  CAS  PubMed  Google Scholar 

  44. Laughlin GA, Ix JH, Cummins K, et al. Extremes of an aromatase index predict increased 25-year risk of cardiovascular mortality in older women. Clin Endocrinol. 2012;77(3):391–8.

    Article  CAS  Google Scholar 

  45. Lee HK, Lee JK, Cho B. The role of androgen in the adipose tissue of males. World J Mens Health. 2013;31:136–40.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Tong G, Hua X, Zhong Y, et al. Intensive insulin therapy increases sex hormone-binding globulin in newly diagnosed type 2 diabetic patients. Eur J Endocrinol. 2014;170(2):237–45.

    Article  CAS  PubMed  Google Scholar 

  47. Armamento-Villareal R, Aguirre LE, Qualls C, et al. Effect of lifestyle intervention on the hormonal profile of frail, obese older men. J Nutr Health Aging. 2016;20(3):334–40.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Mukhin IV, Ignatenko GA, Nikolenko VY. Dyshormonal disorders in gout: experimental and clinical studies. Bull Exp Biol Med. 2002;133(5):491–3.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The authors thank all the endocrinologists, surgeons, and nutritionists of the Multidisciplinary Group in the National Metabolic Management Center of our hospital.

Funding

This project was supported by the Shanghai Committee of Science and Technology of China (Grant No. 17DZ1910603), Fundamental Research Funds for the Central Universities (1501219107), and National Natural Science Foundation of China (NSFC 81500650, 81700752, 81570782).

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Author notes

  1. Cuiling Zhu and Yi Zhang contributed equally to this work.

Authors and Affiliations

  1. Department of Endocrinology and Metabolism, Shanghai Tenth People’s Hospital, School of Medicine, Tongji University, No. 301 Middle Yanchang Road, Shanghai, 200072, China

    Cuiling Zhu, Jingyang Gao, Fangyun Mei, Bing Zhu & Shen Qu

  2. National Metabolic Management Center, Shanghai, 200072, China

    Cuiling Zhu, Jingyang Gao, Fangyun Mei, Bing Zhu & Shen Qu

  3. Laboratory of Endocrinology and Metabolism, West China Hospital of Sichuan University, Chengdu, 610041, China

    Yi Zhang

  4. Department of Endocrinology, Changzhou Cancer Hospital, Soochow University, Changzhou, 213032, Jiangsu, China

    Ling Zhang

  5. Department of Gastrointestinal Surgery, Shanghai Tenth People’s Hospital, School of Medicine, Tongji University, Shanghai, 200072, China

    Liesheng Lu & Donglei Zhou

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  1. Cuiling Zhu
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Contributions

• Study design, data analysis, and draft of the work: Cuiling Zhu and Yi Zhang

• Data collection for the work: Ling Zhang, Fangyun Mei, Jingyang Gao, and Bing Zhu

• Performing the surgery and discussing the manuscript: Liesheng Lu and Donglei Zhou

• Final approval of the version to be published: Shen Qu

All the authors take responsibility for the content of this study.

Corresponding author

Correspondence to Shen Qu.

Ethics declarations

Informed consent was obtained from all individual participants of the study. The study was approved by the ethics committee of the Shanghai Tenth People’s Hospital of Tongji University.

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The authors declare that they have no conflict of interest.

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Zhu, C., Zhang, Y., Zhang, L. et al. Changes in Sex Hormones After Laparoscopic Sleeve Gastrectomy in Chinese Obese Men: a 12-Month Follow-Up. OBES SURG 29, 869–877 (2019). https://doi.org/10.1007/s11695-018-3611-3

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  • DOI: https://doi.org/10.1007/s11695-018-3611-3

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