Home Long-term follow-up of gonadal dysfunction in morbidly obese adolescent boys after bariatric surgery
Article
Licensed
Unlicensed Requires Authentication

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 and Ilene Fennoy EMAIL logo
Published/Copyright: October 23, 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.2010-2724Search 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/dc06-1426Search 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.xSearch 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.2007-2177Search 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.3901391Search 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/dc09-1649Search 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-45-6-1211Search 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.Search 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.2010.202Search 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.2005-0438Search 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.0803691Search 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.2010.07.026Search 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.12018Search 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-2007-1014845Search 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.2013-1173Search 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;2011:906384.10.1155/2011/906384Search 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.2013.12.046Search 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/BF00280883Search 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.S2.555Search 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.2007.06.004Search 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/dmx012Search 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-2012-0398Search 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.122365Search 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.2009.06.007Search 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;2014:190945.10.1155/2014/190945Search 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.2014-1452Search 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-14-0596Search 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.2011.05.007Search 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.2013.02.039Search 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.2006.01.005Search 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.Search 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.xSearch 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.84.10.6082Search 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/JCI119595Search 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.2006-1864Search 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

Articles in the same Issue

  1. Frontmatter
  2. Original Articles
  3. Carotid intima media thickness and associations with serum osteoprotegerin and s-RANKL in children and adolescents with type 1 diabetes mellitus with increased risk for endothelial dysfunction
  4. Cardiometabolic risk factors in preschool children with abdominal obesity from Medellín, Colombia
  5. Long-term follow-up of gonadal dysfunction in morbidly obese adolescent boys after bariatric surgery
  6. Prevalence of overweight and obesity and anthropometric reference centiles for Albanian children and adolescents living in four Balkan nation-states
  7. High urate concentration is associated with elevated blood pressure in schoolchildren
  8. The association of hs-CRP and fibrinogen with anthropometric and lipid parameters in non-obese adolescent girls with polycystic ovary syndrome
  9. Leptin and adiposity as mediators on the association between early puberty and several biomarkers in European adolescents: the HELENA Study
  10. Adolescents with premenstrual syndrome: not only what you eat but also how you eat matters!
  11. Thyroid dysfunction in children with leukemia over the first year after hematopoietic stem cell transplantation
  12. Morning vs. bedtime levothyroxine administration: what is the ideal choice for children?
  13. Basal characteristics and first year responses to human growth hormone (GH) vary according to diagnostic criteria in children with non-acquired GH deficiency (naGHD): observations from a single center over a period of five decades
  14. The prevalence and volumetry of pituitary cysts in children with growth hormone deficiency and idiopathic short stature
  15. SHOX gene deletion screening by FISH in children with short stature and Madelung deformity and their characteristics
  16. FGFR3-related hypochondroplasia: longitudinal growth in 57 children with the p.Asn540Lys mutation
  17. Case Reports
  18. A variable course of Cushing’s disease in a 7 year old: diagnostic dilemma
  19. Severe hyperchylomicronemia in two infants with novel APOC2 gene mutation
Downloaded on 28.9.2025 from https://www.degruyterbrill.com/document/doi/10.1515/jpem-2018-0261/html
Scroll to top button