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Licensed Unlicensed Requires Authentication Published by De Gruyter October 26, 2022

Insights into the implication of obesity in hypogonadism among adolescent boys

  • Mona M. Hassan , Azza M. Sarry Eldin , Noha Musa , Khaled H. El-Wakil , May Ali and Hanaa H. Ahmed EMAIL logo

Abstract

Objectives

This research aimed at uncovering the mechanisms behind obesity-related hypogonadism in adolescent boys and to investigate the association between anthropometric characteristics and testicular functions of these boys.

Methods

This study included 60 adolescent boys (12–18 years) with exogenous obesity (BMI≥95th percentile) and 30 age matched lean controls (BMI=15th–85th percentile). Full clinical examination, anthropometric measurements and pubertal assessment were performed. Laboratory investigations included hemoglobin, hematocrit, lipid panel, LH, FSH, free and total testosterone, inhibin B and estradiol.

Results

The results indicated the presence of positive family history of obesity in 85% of obese boys vs. 40% of the lean counterparts. Concerning SBP of obese boys, 7% were hypertensive (95th percentile), 25% were prehypertensive (between 90th and 95th percentiles) while, DBP findings showed that 33% are hypertensive and 33% are prehypertensive. Meanwhile, 13.3% of lean controls were prehypertensive. Anthropometric measurements and lipid profile values revealed a significant difference between obese and lean boys. Compared to obese boys the normal weight boys had higher levels of free testosterone (21.15 ± 2.90 pg/mL vs. 11.38 ± 3.96 pg/mL, p<0.001), total testosterone (10.59 ± 6.63 ng/dL vs. 3.23 ± 1.70 ng/dL, p<0.001), FSH (7.33 ± 3.75 mIU/mL vs. 5.63 ± 3.96 mIU/mL, p=0.026) and inhibin B (83.28 ± 27.66 pg/mL vs. 62.90 ± 17.85 pg/mL, p=0.001) and they registered lower level of estradiol (18.48 ± 7.33 pg/mL vs. 40.20 ± 7.91 pg/mL, p<0.001). In obese boys, BMI SDS significantly correlated with lipid profile and estradiol whereas, it showed significant negative correlation with LH, free and total testosterone and inhibin B. Penile length significantly correlated with LH while it revealed significant negative correlation with cholesterol.

Conclusions

This study evidenced a close association between obesity and hypogonadism in adolescent boys which could be due to the increased estradiol level and decreased T/E2 ratio.


Corresponding author: Prof. Hanaa H. Ahmed, Professor of Hormones, Hormones Department, Medical Research and Clinical Studies Institute, National Research Centre, 33 El-Bohouth St. (former El-Tahrir St), Dokki, Giza, 12622, Egypt, Phone: 202 33371615, Fax: 202 33370931, E-mail:

Funding source: National Research Centre

  1. Research funding: This work was financially supported by the National Research Centre, Egypt (Thesis fund).

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

  3. Competing interests: Authors state no conflict of interest.

  4. Informed consent: The informed consent was obtained from each participant and his parents after explaining the study design.

  5. Ethical approval: The protocol of this study was approved by the Ethical Committee for Medical Research of the National Research Centre, Egypt (code 14/106).

References

1. Bharti, A, Kushwaha, A. Prevalence of obesity and its associated sociodemographic factors among adolescents in Udham Singh Nagar, Uttarakhand, India. TPI 2021;10:135–41. https://doi.org/10.22271/tpi.2021.v10.i6b.7812.Search in Google Scholar

2. Wang, H. Analyzing neck circumference as a tool for evaluating overweight and obesity in Chinese adolescents. J Healthc Eng 2021;2021:1274627. https://doi.org/10.1155/2021/1274627.Search in Google Scholar PubMed PubMed Central

3. Femila, D, Jansi, RS. Prevalence of obesity and its associated factors among adolescents studying in urban schools. TNNMC J Commun Heal Nurs 2020;8:4–7.Search in Google Scholar

4. Patton, GC, Sawyer, SM, Santelli, JS, Ross, DA, Afifi, R, Allen, NB, et al.. Our future: a Lancet commission on adolescent health and wellbeing. Lancet 2016;387:2423–78. https://doi.org/10.1016/s0140-6736(16)00579-1.Search in Google Scholar PubMed PubMed Central

5. Currie, C, Ahluwalia, N, Godeau, E, Nic Gabhainn, S, Due, P, Currie, DB. Is obesity at individual and national level associated with lower age at menarche? Evidence from 34 countries in the Health Behaviour in School-aged Children Study. J Adolesc Health 2012;50:621–6. https://doi.org/10.1016/j.jadohealth.2011.10.254.Search in Google Scholar PubMed

6. Lian, Q, Mao, Y, Luo, S, Zhang, S, Tu, X, Zuo, X, et al.. Puberty timing associated with obesity and central obesity in Chinese Han girls. BMC Pediatr 2019;19:1. https://doi.org/10.1186/s12887-018-1376-4.Search in Google Scholar PubMed PubMed Central

7. Barcellos Gemelli, IF, Farias Edos, S, Souza, OF. Age at menarche and its association with excess weight and body fat percentage in girls in the Southwestern Region of the Brazilian Amazon. J Pediatr Adolesc Gynecol 2016;29:482–8. https://doi.org/10.1016/j.jpag.2016.02.011.Search in Google Scholar PubMed

8. Herman-Giddens, ME, Steffes, J, Harris, D, Slora, E, Hussey, M, Dowshen, SA, et al.. Secondary sexual characteristics in boys: data from the pediatric research in office settings network. Pediatrics 2012;130:e1058–68. https://doi.org/10.1542/peds.2011-3291.Search in Google Scholar PubMed

9. De Leonibus, C, Marcovecchio, ML, Chiavaroli, V, de Giorgis, T, Chiarelli, F, Mohn, A. Timing of puberty and physical growth in obese children: a longitudinal study in boys and girls. Pediatr Obes 2014;9:292–9. https://doi.org/10.1111/j.2047-6310.2013.00176.x.Search in Google Scholar PubMed

10. Kleber, M, Schwarz, A, Reinehr, T. Obesity in children and adolescents: relationship to growth, pubarche, menarche, and voice break. J Pediatr Endocrinol Metab 2011;24:125–30. https://doi.org/10.1515/jpem.2011.089.Search in Google Scholar PubMed

11. Crocker, MK, Stern, EA, Sedaka, NM, Shomaker, LB, Brady, SM, Ali, AH, et al.. Sexual dimorphisms in the associations of BMI and body fat with indices of pubertal development in girls and boys. J Clin Endocrinol Metab 2014;99:E1519–29. https://doi.org/10.1210/jc.2014-1384.Search in Google Scholar PubMed PubMed Central

12. Novak, JM, Bruzek, J, Zamrazilova, H, Vankova, M, Hill, M, Sedlak, P. The relationship between adolescent obesity and pelvis dimensions in adulthood: a retrospective longitudinal study. PerJ 2020;8:e8951. https://doi.org/10.7717/peerj.8951.Search in Google Scholar PubMed PubMed Central

13. Vandewalle, S, De Schepper, J, Kaufman, JM. Androgens and obesity in male adolescents. Curr Opin Endocrinol Diabetes Obes 2015;22:230–7. https://doi.org/10.1097/med.0000000000000160.Search in Google Scholar

14. Mah, PM, Wittert, GA. Obesity and testicular function. Mol Cell Endocrinol 2010;316:180–6. https://doi.org/10.1016/j.mce.2009.06.007.Search in Google Scholar PubMed

15. Akingbemi, BT. Estrogen regulation of testicular function. Reprod Biol Endocrinol 2005;3:51. https://doi.org/10.1186/1477-7827-3-51.Search in Google Scholar PubMed PubMed Central

16. Pauli, EM, Legro, RS, Demers, LM, Kunselman, AR, Dodson, WC, Lee, PA. Diminished paternity and gonadal function with increasing obesity in men. Fertil Steril 2008;90:346–51. https://doi.org/10.1016/j.fertnstert.2007.06.046.Search in Google Scholar PubMed PubMed Central

17. Lewis, K, Lee, PA. Endocrinology of male puberty. Curr Opin Endocrinol Diabetes Obes 2009;16:5–9. https://doi.org/10.1097/med.0b013e32832029be.Search in Google Scholar PubMed

18. Chada, M, Prusa, R, Bronsky, J, Kotaska, K, Sidlova, K, Pechova, M, et al.. Inhibin B, follicle stimulating hormone, luteinizing hormone and testosterone during childhood and puberty in males: changes in serum concentrations in relation to age and stage of puberty. Physiol Res 2003;52:45–51.10.33549/physiolres.930292Search in Google Scholar

19. Winters, SJ, Wang, C, Abdelrahaman, E, Hadeed, V, Dyky, MA, Brufsky, A. Inhibin B levels in healthy young adult men and prepubertal boys: is obesity the cause for the contemporary decline in sperm count because of fewer Sertoli cells? J Androl 2006;27:560–4. https://doi.org/10.2164/jandrol.05193.Search in Google Scholar PubMed

20. Ghalli, I, Salah, N, Hussien, F, Erfan, M, El-Ruby, M, Mazen, I, et al.. Egyptian growth curves for infants, children and adolescents. In: Sartorio, A, Buckler, JMH, Marazzi, N, editors. Crecere nel mondo. Italy: Ferring Publisher; 2008.Search in Google Scholar

21. Marshall, WA, Tanner, JM. Variations in the pattern of pubertal changes in boys. Arch Dis Child 1970;45:13–23. https://doi.org/10.1136/adc.45.239.13.Search in Google Scholar PubMed PubMed Central

22. Promodu, K, Shanmughadas, KV, Bhat, S, Nair, KR. Penile length and circumference: an Indian study. Int J Impot Res 2007;19:558–63. https://doi.org/10.1038/sj.ijir.3901569.Search in Google Scholar PubMed

23. Fuse, H, Takahara, M, Ishii, H, Sumiya, H, Shimazaki, J. Measurement of testicular volume by ultrasonography. Int J Androl 1990;13:267–72. https://doi.org/10.1111/j.1365-2605.1990.tb01031.x.Search in Google Scholar PubMed

24. Chipkevitch, E, Nishimura, RT, Tu, DG, Galea-Rojas, M. Clinical measurement of testicular volume in adolescents: comparison of the reliability of 5 methods. J Urol 1996;156:2050–3. https://doi.org/10.1016/s0022-5347(01)65433-8.Search in Google Scholar

25. Goede, J, Hack, WW, Sijstermans, K, van der Voort-Doedens, LM, Van der Ploeg, T, Meij-de Vries, A, et al.. Normative values for testicular volume measured by ultrasonography in a normal population from infancy to adolescence. Horm Res Paediatr 2011;76:56–64. https://doi.org/10.1159/000326057.Search in Google Scholar PubMed

26. Uotila, M, Ruoslahti, E, Engvall, E. Two-site sandwich enzyme immunoassay with monoclonal antibodies to human alpha-fetoprotein. J Immunol Methods 1981;42:11–5. https://doi.org/10.1016/0022-1759(81)90219-2.Search in Google Scholar PubMed

27. Styne, DM. Laboratory values for pediatric endocrinology. In: Pediatric endocrinology. Cham: Springer; 2016:385–434 pp.10.1007/978-3-319-18371-8_16Search in Google Scholar

28. Rebar, RW, Erickson, GF, Yen, SS. Idiopathic premature ovarian failure: clinical and endocrine characteristics. Fertil Steril 1982;37:35–41. https://doi.org/10.1016/s0015-0282(16)45973-x.Search in Google Scholar

29. Endocrine sciences. Endocrine sciences. In: Endocrinology expected values and S.I. unit conversion tables. 4301 lost Hills Road, Calabasas Hills, CA 91301: Laboratory Corporation of America; 2015:1–80 pp.Search in Google Scholar

30. Winters, SJ, Kelley, DE, Goodpaster, B. The analog free testosterone assay: are the results in men clinically useful? Clin Chem 1998;44:2178–82. https://doi.org/10.1093/clinchem/44.10.2178.Search in Google Scholar

31. Lee, JM, Wasserman, R, Kaciroti, N, Gebremariam, A, Steffes, J, Dowshen, S, et al.. Timing of puberty in overweight versus obese boys. Pediatrics 2016;137:e20150164. https://doi.org/10.1542/peds.2015-0164.Search in Google Scholar PubMed

32. Tietz, NW. Textbook of clinical chemistry. Co. Philadelphia: WB Saunders; 1986:1919 p.Search in Google Scholar

33. Tietz, NW. Clinical guide to laboratory tests, 3rd ed. Philadelphia: WB Saunders; 1995:268–73 pp.Search in Google Scholar

34. Wang, Y. Is obesity associated with early sexual maturation? A comparison of the association in American boys versus girls. J Pediatr 2002;110:903–10. https://doi.org/10.1542/peds.110.5.903.Search in Google Scholar PubMed

35. Fejes, I, Koloszar, S, Zavaczki, Z, Daru, J, Szöllösi, J, Pal, A. Effect of body weight on testosterone/estradiol ratio in oligozoospermic patients. Arch Androl 2006;52:97–102. https://doi.org/10.1080/01485010500315479.Search in Google Scholar PubMed

36. de Boer, H, Verschoor, L, Ruinemans-Koerts, J, Jansen, M. Letrozole normalizes serum testosterone in severely obese men with hypogonadotropic hypogonadism. Diabetes Obes Metabol 2005;7:211–5. https://doi.org/10.1111/j.1463-1326.2004.00397.x.Search in Google Scholar PubMed

37. Gillson, G, Marsden, T. “You’ve hit menopause. Now what?” 2nd ed. 3 simple steps to restoring hormone balance. In: Chapter on: Male hormone balance. Rocky Mountain Analytical Corp.; 2004;118–48 pp.Search in Google Scholar

38. Teerds, KJ, de Rooij, DG, Keijer, J. Functional relationship between obesity and male reproduction: from humans to animal models. Hum Reprod Update 2011;17:667–83. https://doi.org/10.1093/humupd/dmr017.Search in Google Scholar PubMed

39. Shao, Y, Zeng, R, Yao, Q, Fan, K, Jing, J, Ge, YF, et al.. Waist-hip ratio correlates with the levels of reproductive endocrine hormones in abdominally obese males. Zhonghua Nan Ke Xue 2013;19:634–6.Search in Google Scholar

40. Mermer, M, Akdevelioğlu, Y. The role of obesity in male fertility. Int J Reprod Contracept Obstet Gynecol 2018;7:3435–40. https://doi.org/10.18203/2320-1770.ijrcog20183749.Search in Google Scholar

41. Radicioni, AF, Anzuini, A, De Marco, E, Nofroni, I, Castracane, VD, Lenzi, A. Changes in serum inhibin B during normal male puberty. Eur J Endocrinol 2005;152:403–9. https://doi.org/10.1530/eje.1.01855.Search in Google Scholar PubMed

42. Aggerholm, AS, Thulstrup, AM, Toft, G, Ramlau-Hansen, CH, Bonde, JP. Is overweight a risk factor for reduced semen quality and altered serum sex hormone profile? Fertil Steril 2008;90:619–26. https://doi.org/10.1016/j.fertnstert.2007.07.1292.Search in Google Scholar PubMed

43. Fu, JF, Dong, GP, Liang, L, Jiang, YJ, Chen, LQ, Dayan, C. Early activation of the inhibin B/FSH axis in obese Tanner stage G1PH1 boys. Clin Endocrinol (Oxf) 2006;65:327–32. https://doi.org/10.1111/j.1365-2265.2006.02597.x.Search in Google Scholar PubMed

44. Wang, F, Vihma, V, Soronen, J, Turpeinen, U, Hämäläinen, E, Savolainen-Peltonen, H, et al.. 17β-estradiol and estradiol fatty acyl esters and estrogen-converting enzyme expression in adipose tissue in obese men and women. J Clin Endocrinol Metab 2013;98:4923–31. https://doi.org/10.1210/jc.2013-2605.Search in Google Scholar PubMed

45. Zumoff, B, Strain, GW, Kream, J, O’Connor, J, Levin, J, Fukushima, DK. Obese young men have elevated plasma estrogen levels but obese premenopausal women do not. Metabolism 1981;30:1011–4. https://doi.org/10.1016/0026-0495(81)90102-5.Search in Google Scholar PubMed

46. Rohrmann, S, Shiels, MS, Lopez, DS, Rifai, N, Nelson, WG, Kanarek, N, et al.. Body fatness and sex steroid hormone concentrations in US men: results from NHANES III. Cancer Causes Control 2011;22:1141–51. https://doi.org/10.1007/s10552-011-9790-z.Search in Google Scholar PubMed PubMed Central

47. Schneider, G, Kirschner, MA, Berkowitz, R, Ertel, NH. Increased estrogen production in obese men. J Clin Endocrinol Metab 1979;48:633–8. https://doi.org/10.1210/jcem-48-4-633.Search in Google Scholar PubMed

48. Strain, GW, Zumoff, B, Kream, J, Strain, JJ, Deucher, R, Rosenfeld, RS, et al.. Mild hypogonadotropic hypogonadism in obese men. Metabolism 1982;31:871–5. https://doi.org/10.1016/0026-0495(82)90175-5.Search in Google Scholar PubMed

49. Allen, NE, Appleby, PN, Davey, GK, Key, TJ. Lifestyle and nutritional determinants of bioavailable androgens and related hormones in British men. Cancer Causes Control 2002;13:353–63. https://doi.org/10.1023/a:1015238102830.10.1023/A:1015238102830Search in Google Scholar

50. Al-Ali, MB, Gutschi, T, Pummer, K, Zigeuner, R, Brookman-May, S, Wieland, WF, et al.. Body mass index has no impact on sperm quality but on reproductive hormones levels. Andrologia 2014;46:106–11. https://doi.org/10.1111/and.12051.Search in Google Scholar PubMed

51. Cheraghi, L, Amiri, P, Karimi, M, Mehrabi, Y, Azizi, F. Distribution of body mass index in children with different parental risk: findings of a family-based cohort study in a West-Asian population. Sci Rep 2019;9:9375. https://doi.org/10.1038/s41598-019-45543-y.Search in Google Scholar PubMed PubMed Central

52. Ostchega, Y, Carroll, M, Prineas, RJ, McDowell, MA, Louis, T, Tilert, T. Trends of elevated blood pressure among children and adolescents: data from the National Health and Nutrition Examination Survey 1988–2006. Am J Hypertens 2009;22:59–67. https://doi.org/10.1038/ajh.2008.312.Search in Google Scholar PubMed

53. Milyani, AA, Al-Agha, AE. The effect of body mass index and gender on lipid profile in children and adolescents in Saudi Arabia. Ann Afr Med 2019;18:42–6. https://doi.org/10.4103/aam.aam_17_18.Search in Google Scholar PubMed PubMed Central

54. Zirkin, BR, Papadopoulos, V. Leydig cells: formation, function, and regulation. Biol Reprod 2018;99:101–11. https://doi.org/10.1093/biolre/ioy059.Search in Google Scholar PubMed PubMed Central

55. Wang, HJ, Wang, Q, Lv, ZM, Wang, CL, Li, CP, Rong, YL. Resveratrol appears to protect against oxidative stress and steroidogenesis collapse in mice fed high-calorie and high-cholesterol diet. Andrologia 2015;47:59–65. https://doi.org/10.1111/and.12231.Search in Google Scholar PubMed

56. Zhao, JL, Zhao, YY, Zhu, WJ. A high-fat, high-protein diet attenuates the negative impact of casein-induced chronic inflammation on testicular steroidogenesis and sperm parameters in adult mice. Gen Comp Endocrinol 2017;252:48–59. https://doi.org/10.1016/j.ygcen.2017.07.013.Search in Google Scholar PubMed

57. Zhang, YD, Tan, LN, Luo, SY, Chen, YX, Wei, HY. Status of penis and testicular development and effects of overweight/obesity on them in boys in the Zhengzhou area. Zhong Guo Dang Dai Er Ke Za Zhi 2015;17:72–6.Search in Google Scholar

58. Andersen, I, Heitmann, BL, Wagner, G. Obesity and sexual dysfunction in younger Danish men. J Sex Med 2008;5:2053–60. https://doi.org/10.1111/j.1743-6109.2008.00920.x.Search in Google Scholar PubMed

59. Najafi, M, Yousefi, A, Kumar, SC, Malini, SS. Diminished fertility in men with increased BMI. J Paramed Sci 2011;2:42–7.Search in Google Scholar

60. Esposito, K, Giugliano, F, Di Palo, C, Giugliano, G, Marfella, R, D’Andrea, F, et al.. Effect of lifestyle changes on erectile dysfunction in obese men: a randomized controlled trial. JAMA 2004;291:2978–84. https://doi.org/10.1001/jama.291.24.2978.Search in Google Scholar PubMed

Received: 2022-05-26
Accepted: 2022-10-03
Published Online: 2022-10-26
Published in Print: 2022-12-16

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