Startseite Long-term follow-up of gonadal dysfunction in morbidly obese adolescent boys after bariatric surgery
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Long-term follow-up of gonadal dysfunction in morbidly obese adolescent boys after bariatric surgery

  • Vivian L. Chin , Kristen M. Willliams , Tegan Donnelley , Marisa Censani ORCID logo , Rushika Conroy , Shulamit Lerner , Sharon E. Oberfield , Donald J. McMahon , Jeffrey Zitsman und Ilene Fennoy EMAIL logo
Veröffentlicht/Copyright: 23. Oktober 2018

Abstract

Background

Elevated body mass index (BMI) is associated with hypogonadism in men but this is not well described in adolescents. The aim is to evaluate gonadal dysfunction and the effects of weight loss after gastric banding in obese adolescent boys.

Methods

Thirty-seven of 54 boys (age 16.2±1.2 years, mean BMI 48.2 kg/m2) enrolled at the Center for Adolescent Bariatric Surgery at Columbia University Medical Center had low total testosterone for Tanner 5 <350 ng/dL. Sixteen had long-term hormonal data for analysis at baseline (T0), 1 year (T1) and 2 years (T2) post-surgery. T-tests, chi-squared (χ2) tests, correlation and linear mixed models were performed.

Results

At T0, the hypogonadal group had higher systolic blood pressure (SBP) (75th vs. 57th percentile, p=0.02), fasting insulin (19 vs. 9 μIU/mL, p=0.0008) and homeostatic index of insulin resistance (HOMA-IR) (4.2 vs. 1.9, p=0.009) compared to control group. Total testosterone was negatively correlated with fasting insulin and HOMA-IR. In the long-term analysis, BMI, weight, waist circumference (WC), and % excess weight decreased at T1 and T2 compared to T0. Mean total testosterone at T0, T1 and T2 were 268, 304 and 368 ng/dL, respectively (p=0.07). There was a statistically significant negative correlation between BMI and testosterone after 2 years (r=−0.81, p=0.003).

Conclusions

Low testosterone levels but unaltered gonadotropins are common in this group and associated with insulin resistance. While a significant increase in testosterone was not found over time, the negative relationship between BMI and testosterone persisted, suggesting there may be an optimal threshold for testosterone production with respect to BMI. Long-term studies are needed.


Corresponding author: Ilene Fennoy, MD, MPH, Department of Pediatrics, Division of Pediatric Endocrinology, Columbia University Medical Center, 622 West 168th Street, PH 17W-307, New York, NY 10032, USA, Phone: (+212) 305-6559, Fax: (+212) 305-4778
aVivian L. Chin and Kristen M. Willliams contributed equally.bPresent affiliation: SUNY Downstate Medical Center, Brooklyn, NY, USA.cPresent affiliation: Weill Cornell University Medical Center, NY, USA.dPresent affiliation: Baystate Medical Center, Springfield, MA, USA.ePresent affiliation: Healthy Horizons Pediatric Endocrinology, Riverdale, NY, USA.

Acknowledgments

This work was supported by National Institutes of Health (NIH) Grant NIDDK T32 DK 06552 (PI Sharon Oberfield). Baseline data analysis was previously presented at the 95th Annual Endocrine Society Meeting, San Francisco, CA, June 2013, and follow-up analysis was presented at the 10th International Meeting of Pediatric Endocrinology held during September 2017 in Washington, DC. We would like to thank Chengchen Zhang for her help with statistical analysis.

  1. Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.

  2. Research funding: U.S. Department of Health and Human Services, National Institutes of Health, NIH Clinical Center, NIH Grant NIDDK T32 DK 06552, Funder Id: 10.13039/100000098.

  3. Employment or leadership: None declared.

  4. Honorarium: None declared.

  5. Competing interests: Dr. Oberfield reports grants from NIH/NIDDK (U.S. Department of Health and Human Services, National Institutes of Health, NIH Clinical Center, NIH Grant NIDDK T32 DK 06552) during the conduct of the study. Dr. Fennoy reports grants and personal fees from Novo Nordisk, and personal fees from Island Peer Review Organization outside the submitted work. The other authors have no financial relationships or conflicts of interest to disclose.

References

1. Dandona P, Dhindsa S. Update: hypogonadotropic hypogonadism in type 2 diabetes and obesity. J Clin Endocrinol Metab 2011;96:2643–51.10.1210/jc.2010-2724Suche in Google Scholar PubMed PubMed Central

2. Kapoor D, Aldred H, Clark S, Channer KS, Jones TH. Clinical and biochemical assessment of hypogonadism in men with type 2 diabetes: correlations with bioavailable testosterone and visceral adiposity. Diabetes Care 2007;30:911–7.10.2337/dc06-1426Suche in Google Scholar PubMed

3. Rhoden EL, Ribeiro EP, Teloken C, Souto CA. Diabetes mellitus is associated with subnormal serum levels of free testosterone in men. BJU Int 2005;96:867–70.10.1111/j.1464-410X.2005.05728.xSuche in Google Scholar PubMed

4. Grossmann M, Thomas MC, Panagiotopoulos S, Sharpe K, Macisaac RJ, et al. Low testosterone levels are common and associated with insulin resistance in men with diabetes. J Clin Endocrinol Metab 2008;93:1834–40.10.1210/jc.2007-2177Suche in Google Scholar PubMed

5. Corona G, Mannucci E, Petrone L, Ricca V, Balercia G, et al. Association of hypogonadism and type II diabetes in men attending an outpatient erectile dysfunction clinic. Int J Impot Res 2006;18:190–7.10.1038/sj.ijir.3901391Suche in Google Scholar PubMed

6. Dhindsa S, Miller MG, McWhirter CL, Mager DE, Ghanim H, et al. Testosterone concentrations in diabetic and nondiabetic obese men. Diabetes Care 2010;33:1186–92.10.2337/dc09-1649Suche in Google Scholar PubMed PubMed Central

7. Glass AR, Swerdloff RS, Bray GA, Dahms WT, Atkinson RL. Low serum testosterone and sex-hormone-binding-globulin in massively obese men. J Clin Endocrinol Metab 1977;45:1211–9.10.1210/jcem-45-6-1211Suche in Google Scholar PubMed

8. Ogden CL CM, Kit BK. Prevalence of obesity in the United States, 2009–10. Hyattsville, MD: US Department of Health and Human Services, CDC, National Center for Health Statistics, 2012.Suche in Google Scholar

9. Moriarty-Kelsey M, Harwood JE, Travers SH, Zeitler PS, Nadeau KJ. Testosterone, obesity and insulin resistance in young males: evidence for an association between gonadal dysfunction and insulin resistance during puberty. J Pediatr Endocrinol Metab 2010;23:1281–7.10.1515/jpem.2010.202Suche in Google Scholar PubMed PubMed Central

10. Reinehr T, de Sousa G, Roth CL, Andler W. Androgens before and after weight loss in obese children. J Clin Endocrinol Metab 2005;90:5588–95.10.1210/jc.2005-0438Suche in Google Scholar PubMed

11. Denzer C, Weibel A, Muche R, Karges B, Sorgo W, et al. Pubertal development in obese children and adolescents. Int J Obes (Lond) 2007;31:1509–19.10.1038/sj.ijo.0803691Suche in Google Scholar PubMed

12. Taneli F, Ersoy B, Ozhan B, Calkan M, Yilmaz O, et al. The effect of obesity on testicular function by insulin-like factor 3, inhibin B, and leptin concentrations in obese adolescents according to pubertal stages. Clin Biochem 2010;43:1236–40.10.1016/j.clinbiochem.2010.07.026Suche in Google Scholar PubMed

13. Mogri M, Dhindsa S, Quattrin T, Ghanim H, Dandona P. Testosterone concentrations in young pubertal and post-pubertal obese males. Clin Endocrinol (Oxf) 2013;78:593–9.10.1111/cen.12018Suche in Google Scholar PubMed PubMed Central

14. Pintor C, Loche S, Faedda A, Fanni V, Nurchi AM, et al. Adrenal androgens in obese boys before and after weight loss. Horm Metab Res 1984;16:544–8.10.1055/s-2007-1014845Suche in Google Scholar PubMed

15. Reinehr T, Kulle A, Wolters B, Lass N, Welzel M, et al. Steroid hormone profiles in prepubertal obese children before and after weight loss. J Clin Endocrinol Metab 2013;98:E1022–30.10.1210/jc.2013-1173Suche in Google Scholar PubMed

16. Conroy R, Lee EJ, Jean A, Oberfield SE, Sopher A, et al. Effect of laparoscopic adjustable gastric banding on metabolic syndrome and its risk factors in morbidly obese adolescents. J Obes 2011;2011:906384.10.1155/2011/906384Suche in Google Scholar PubMed PubMed Central

17. Chin V, Censani M, Lerner S, Conroy R, Oberfield S, et al. Gonadal dysfunction in morbidly obese adolescent girls. Fertil Steril 2014;101:1142–8.10.1016/j.fertnstert.2013.12.046Suche in Google Scholar PubMed PubMed Central

18. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, et al. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 1985;28:412–9.10.1007/BF00280883Suche in Google Scholar PubMed

19. National High Blood Pressure Education Program Working Group on High Blood Pressure in C, Adolescents. The fourth report on the diagnosis, evaluation, and treatment of high blood pressure in children and adolescents. Pediatrics 2004;114(2 Suppl 4th Report):555–76.10.1542/peds.114.S2.555Suche in Google Scholar PubMed

20. Cook S, Auinger P, Li C, Ford ES. Metabolic syndrome rates in United States adolescents, from the National Health and Nutrition Examination Survey, 1999–2002. J Pediatr 2008;152:165–70.10.1016/j.jpeds.2007.06.004Suche in Google Scholar PubMed

21. Escobar-Morreale HF, Santacruz E, Luque-Ramirez M, Botella Carretero JI. Prevalence of ’obesity-associated gonadal dysfunction’ in severely obese men and women and its resolution after bariatric surgery: a systematic review and meta-analysis. Hum Reprod Update 2017;23:390–408.10.1093/humupd/dmx012Suche in Google Scholar PubMed

22. Zhai L, Zhao J, Bai Y, Liu L, Zheng L, et al. Sexual development in prepubertal obese boys: a 4-year longitudinal study. J Pediatr Endocrinol Metab 2013;26:895–901.10.1515/jpem-2012-0398Suche in Google Scholar PubMed

23. Fui MN, Dupuis P, Grossmann M. Lowered testosterone in male obesity: mechanisms, morbidity and management. Asian J Androl 2014;16:223–31.10.4103/1008-682X.122365Suche in Google Scholar PubMed PubMed Central

24. Mah PM, Wittert GA. Obesity and testicular function. Mol Cell Endocrinol 2010;316:180–6.10.1016/j.mce.2009.06.007Suche in Google Scholar PubMed

25. Zhao J, Zhai L, Liu Z, Wu S, Xu L. Leptin level and oxidative stress contribute to obesity-induced low testosterone in murine testicular tissue. Oxid Med Cell Longev 2014;2014:190945.10.1155/2014/190945Suche in Google Scholar PubMed PubMed Central

26. Vandewalle S, Taes Y, Fiers T, Van Helvoirt M, Debode P, et al. Sex steroids in relation to sexual and skeletal maturation in obese male adolescents. J Clin Endocrinol Metab 2014;99:2977–85.10.1210/jc.2014-1452Suche in Google Scholar PubMed

27. Samavat J, Facchiano E, Lucchese M, Forti G, Mannucci E, et al. Hypogonadism as an additional indication for bariatric surgery in male morbid obesity? Eur J Endocrinol 2014;171:555–60.10.1530/EJE-14-0596Suche in Google Scholar PubMed

28. Rao SR, Kini S, Tamler R. Sex hormones and bariatric surgery in men. Gend Med 2011;8:300–11.10.1016/j.genm.2011.05.007Suche in Google Scholar PubMed

29. Luconi M, Samavat J, Seghieri G, Iannuzzi G, Lucchese M, et al. Determinants of testosterone recovery after bariatric surgery: is it only a matter of reduction of body mass index? Fertil Steril 2013;99:1872–9 e1.10.1016/j.fertnstert.2013.02.039Suche in Google Scholar PubMed

30. Alagna S, Cossu ML, Gallo P, Tilocca PL, Pileri P, et al. Biliopancreatic diversion: long-term effects on gonadal function in severely obese men. Surg Obes Relat Dis 2006;2:82–6.10.1016/j.soard.2006.01.005Suche in Google Scholar PubMed

31. Hofstra J, Loves S, van Wageningen B, Ruinemans-Koerts J, Jansen I, et al. High prevalence of hypogonadotropic hypogonadism in men referred for obesity treatment. Neth J Med 2008;66:103–9.Suche in Google Scholar PubMed

32. Ishikawa T, Fujioka H, Ishimura T, Takenaka A, Fujisawa M. Expression of leptin and leptin receptor in the testis of fertile and infertile patients. Andrologia 2007;39:22–7.10.1111/j.1439-0272.2006.00754.xSuche in Google Scholar PubMed

33. Isidori AM, Caprio M, Strollo F, Moretti C, Frajese G, et al. Leptin and androgens in male obesity: evidence for leptin contribution to reduced androgen levels. J Clin Endocrinol Metab 1999;84:3673–80.10.1210/jcem.84.10.6082Suche in Google Scholar PubMed

34. Wabitsch M, Blum WF, Muche R, Braun M, Hube F, et al. Contribution of androgens to the gender difference in leptin production in obese children and adolescents. J Clin Invest 1997;100:808–13.10.1172/JCI119595Suche in Google Scholar PubMed PubMed Central

35. Rosner W, Auchus RJ, Azziz R, Sluss PM, Raff H. Position statement: Utility, limitations, and pitfalls in measuring testosterone: an Endocrine Society position statement. J Clin Endocrinol Metab 2007;92:405–13.10.1210/jc.2006-1864Suche in Google Scholar PubMed

Received: 2018-06-12
Accepted: 2018-09-25
Published Online: 2018-10-23
Published in Print: 2018-11-27

©2018 Walter de Gruyter GmbH, Berlin/Boston

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