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Perspective

Considerations when treating male pubertal delay pharmacologically

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Pages 1903-1914 | Received 29 Dec 2021, Accepted 18 Oct 2022, Published online: 25 Oct 2022

References

  • Howard SR, Dunkel L. Delayed Puberty-Phenotypic diversity, molecular genetic mechanisms, and recent discoveries. Endocr Rev. 2019;40(5):1285–1317.
  • Raivio T, Miettinen PJ. Constitutional delay of puberty versus congenital hypogonadotropic hypogonadism: genetics, management and updates. Best Pract Res Clin Endocrinol Metab. 2019;33(3):101316.
  • Hansen AB, Wojdemann D, Renault CH, et al. DIAGNOSIS OF ENDOCRINE DISEASE: sex steroid action in adolescence: too much, too little; too early, too late. Eur J Endocrinol. 2021;184(1):R17–R28.
  • Spaziani M, Tarantino C, Tahani N, et al. Hypothalamo-Pituitary axis and puberty. Mol Cell Endocrinol. 2021;520:111094.
  • Rey RA. Mini-puberty and true puberty: differences in testicular function. Ann Endocrinol (Paris). 2014;75(2):58–63.
  • Edelsztein NY, Rey RA. Importance of the androgen receptor signaling in gene transactivation and transrepression for pubertal maturation of the testis. Cells. 2019;8(861):1–17.
  • Fukami M. Puberty in patients with aromatase disorders. Curr Opin Endocr Metab Res. 2020;14:1–6.
  • Birzniece V, Ho KKY. MECHANISMS IN ENDOCRINOLOGY: paracrine and endocrine control of the growth hormone axis by estrogen. Eur J Endocrinol. 2021;184(6):R269–R278.
  • Madsen A, Oehme NB, Roelants M, et al. Testicular ultrasound to stratify hormone references in a cross-sectional Norwegian study of male puberty. J Clin Endocrinol Metab. 2020;105(6):1888–1898.
  • Marshall WA, Tanner JM. Variations in the pattern of pubertal changes in boys. Arch Dis Child. 1970;45(239):13–23.
  • Grinspon RP, Bedecarrás P, Ballerini MG, et al. Early onset of primary hypogonadism revealed by serum anti-Müllerian hormone determination during infancy and childhood in trisomy 21. Int J Androl. 2011;34(5pt2):e487–e498.
  • Largo RH, Prader A. Pubertal development in Swiss boys. Helv Paediatr Acta. 1983;38(3):211–228.
  • Roche AF, Wellens R, Attie KM, et al. The timing of sexual maturation in a group of US white youths. J Pediatr Endocrinol Metab. 1995;8(1):11–18.
  • Juul A, Teilmann G, Scheike T, et al. Pubertal development in Danish children: comparison of recent European and US data. Int J Androl. 2006;29(1):247–255. discussion 286-90.
  • Nathan BM, Palmert MR. Regulation and disorders of pubertal timing. Endocrinol Metab Clin North Am. 2005;34(3):617–641. ix.
  • Palmert MR, Dunkel L. Clinical practice delayed puberty. N Engl J Med. 2012;366(5):443–453.
  • Salonia A, Rastrelli G, Hackett G, et al. Paediatric and adult-onset male hypogonadism. Nat Rev Dis Primers. 2019;5(1):38.
  • Galazzi E, Persani LG. Differential diagnosis between constitutional delay of growth and puberty, idiopathic growth hormone deficiency and congenital hypogonadotropic hypogonadism: a clinical challenge for the pediatric endocrinologist. Minerva Endocrinol. 2020;45(4):354–375.
  • Weissberger AJ, Ho KK. Activation of the somatotropic axis by testosterone in adult males: evidence for the role of aromatization. J Clin Endocrinol Metab. 1993;76(6):1407–1412.
  • Veldhuis JD, Metzger DL, Martha PM Jr., et al. Estrogen and testosterone, but not a nonaromatizable androgen, direct network integration of the hypothalamo-somatotrope (growth hormone)-insulin-like growth factor I axis in the human: evidence from pubertal pathophysiology and sex-steroid hormone replacement. J Clin Endocrinol Metab. 1997;82(10):3414–3420.
  • Harrington J, Palmert MR. Clinical review: distinguishing constitutional delay of growth and puberty from isolated hypogonadotropic hypogonadism: critical appraisal of available diagnostic tests. J Clin Endocrinol Metab. 2012;97(9):3056–3067.
  • Mosbah H, Bouvattier C, Maione L, et al. GnRH stimulation testing and serum inhibin B in males: insufficient specificity for discriminating between congenital hypogonadotropic hypogonadism from constitutional delay of growth and puberty. Hum Reprod. 2020;35(10):2312–2322.
  • Sedlmeyer IL, Palmert MR. Delayed puberty: analysis of a large case series from an academic center. J Clin Endocrinol Metab. 2002;87(4):1613–1620.
  • Jonsdottir-Lewis E, Feld A, Ciarlo R, et al. Timing of pubertal onset in girls and boys with constitutional delay. J Clin Endocrinol Metab. 2021;106(9):e3693–e3703.
  • Cassatella D, Howard SR, Acierno JS, et al. Congenital hypogonadotropic hypogonadism and constitutional delay of growth and puberty have distinct genetic architectures. Eur J Endocrinol. 2018;178(4):377–388.
  • Grinspon RP, Freire AV, Rey RA. Hypogonadism in pediatric health: adult medicine concepts fail. Trends Endocrinol Metab. 2019;30(12):879–890.
  • Grinspon RP, Ropelato MG, Bedecarrás P, et al. Gonadotrophin secretion pattern in anorchid boys from birth to pubertal age: pathophysiological aspects and diagnostic usefulness. Clin Endocrinol (Oxf). 2012;76(5):698–705.
  • Grinspon RP, Ropelato MG, Gottlieb S, et al. Basal follicle-stimulating hormone and peak gonadotropin levels after gonadotropin-releasing hormone infusion show high diagnostic accuracy in boys with suspicion of hypogonadotropic hypogonadism. J Clin Endocrinol Metab. 2010;95(6):2811–2818.
  • Chan YM, Lippincott MF, Sales Barroso P, et al. Using kisspeptin to predict pubertal outcomes for youth with pubertal delay. J Clin Endocrinol Metab. 2020;105(8):e2717–e2725.
  • Chaudhary S, Walia R, Bhansali A, et al. FSH stimulated inhibin B (FSH-iB): a novel marker for the accurate prediction of pubertal outcome in delayed puberty. J Clin Endocrinol Metab. 2021;106(9):e3495–e3505.
  • Saengkaew T, Patel HR, Banerjee K, et al. Genetic evaluation supports differential diagnosis in adolescent patients with delayed puberty. Eur J Endocrinol. 2021;185(5):617–627.
  • Federici S, Goggi G, Quinton R, et al. New and consolidated therapeutic options for pubertal induction in hypogonadism: in-depth review of the literature. Endocr Rev. 2022;43(5):824–851. bnab043 (ahead of print).
  • Dwyer AA. Psychosexual effects resulting from delayed, incomplete, or absent puberty. Curr Opin Endocr Metab Res. 2020;14:15–21.
  • Maione L, Pala G, Bouvattier C, et al. Congenital hypogonadotropic hypogonadism/Kallmann syndrome is associated with statural gain in both men and women: a monocentric study. Eur J Endocrinol. 2020;182(2):185.
  • Cangiano B, Goggi G, Federici S, et al. Predictors of reproductive and non-reproductive outcomes of gonadotropin mediated pubertal induction in male patients with congenital hypogonadotropic hypogonadism (CHH). J Endocrinol Invest. 2021;44(11):2445–2454.
  • Varimo T, Miettinen PJ, Kansakoski J, et al. Congenital hypogonadotropic hypogonadism, functional hypogonadotropism or constitutional delay of growth and puberty? An analysis of a large patient series from a single tertiary center. Hum Reprod. 2017;32(1):147–153.
  • Ankarberg-Lindgren C, Norjavaara E. Changes of diurnal rhythm and levels of total and free testosterone secretion from pre to late puberty in boys: testis size of 3 ml is a transition stage to puberty. Eur J Endocrinol. 2004;151(6):747–757.
  • Richman RA, Kirsch LR. Testosterone treatment in adolescent boys with constitutional delay in growth and development. N Engl J Med. 1988;319(24):1563–1567.
  • Bergadá I, Bergadá C. Long term treatment with low dose testosterone in constitutional delay of growth and puberty: effect on bone age maturation and pubertal progression. J Pediatr Endocrinol Metab. 1995;8(2):117–122.
  • Sukumar SP, Bhansali A, Sachdeva N, et al. Diagnostic utility of testosterone priming prior to dynamic tests to differentiate constitutional delay in puberty from isolated hypogonadotropic hypogonadism. Clin Endocrinol (Oxf). 2017;86(5):717–724.
  • Persani L, Bonomi M, Cools M, et al. ENDO-ERN expert opinion on the differential diagnosis of pubertal delay. Endocrine. 2021;71(3):681–688.
  • Vogiatzi M, Tursi JP, Jaffe JS, et al. Testosterone use in adolescent males: current practice and unmet needs. J Endocr Soc. 2021;5(1):bvaa161.
  • Galazzi E, Improda N, Cerbone M, et al. Clinical benefits of sex steroids given as a priming prior to GH provocative test or as a growth-promoting therapy in peripubertal growth delays: results of a retrospective study among ENDO-ERN centres. Clin Endocrinol (Oxf). 2021;94(2):219–228.
  • Stancampiano MR, Lucas-Herald AK, Russo G, et al. Testosterone therapy in adolescent boys: the need for a structured approach. Horm Res Paediatr. 2019;92(4):215–228.
  • Rohayem J, Hauffa BP, Zacharin M, et al. Testicular growth and spermatogenesis: new goals for pubertal hormone replacement in boys with hypogonadotropic hypogonadism? -a multicentre prospective study of hCG/rFSH treatment outcomes during adolescence. Clin Endocrinol (Oxf). 2017;86(1):75–87.
  • Bi Y, Perry PJ, Ellerby M, et al. Population pharmacokinetic/pharmacodynamic modeling of depot testosterone cypionate in healthy male subjects. CPT Pharmacometrics Syst Pharmacol. 2018;7(4):259–268.
  • Varimo T, Huopio H, Kariola L, et al. Letrozole versus testosterone for promotion of endogenous puberty in boys with constitutional delay of growth and puberty: a randomised controlled phase 3 trial. Lancet Child Adolesc Health. 2019;3(2):109–120.
  • Vandewalle S, Van Caenegem E, Craen M, et al. Growth, sexual and bone development in a boy with bilateral anorchia under testosterone treatment guided by the development of his monozygotic twin. J Pediatr Endocrinol Metab. 2018;31(3):361–367.
  • Giagulli VA, Triggiani V, Carbone MD, et al. The role of long-acting parenteral testosterone undecanoate compound in the induction of secondary sexual characteristics in males with hypogonadotropic hypogonadism. J Sex Med. 2011;8(12):3471–3478.
  • Santhakumar A, Miller M, Quinton R. Pubertal induction in adult males with isolated hypogonadotropic hypogonadism using long-acting intramuscular testosterone undecanoate 1-g depot (Nebido). Clin Endocrinol (Oxf). 2014;80(1):155–157.
  • Soliman AT, Khadir MM, Asfour M. Testosterone treatment in adolescent boys with constitutional delay of growth and development. Metabolism. 1995;44(8):1013–1015.
  • Rey RA. Recent advancement in the treatment of boys and adolescents with hypogonadism. Ther Adv Endocrinol Metab. 2021;12:1–17.
  • Schurmeyer T, Nieschlag E. Comparative pharmacokinetics of testosterone enanthate and testosterone cyclohexanecarboxylate as assessed by serum and salivary testosterone levels in normal men. Int J Androl. 1984;7(3):181–187.
  • Di Luigi L, Sgrò P, Romanelli F, et al. Urinary and serum hormones profiles after testosterone enanthate administration in male hypogonadism: concerns on the detection of doping with testosterone in treated hypogonadal athletes. J Endocrinol Invest. 2009;32(5):445–453.
  • Ekström L, Schulze JJ, Guillemette C, et al. Bioavailability of testosterone enanthate dependent on genetic variation in the phosphodiesterase 7B but not on the uridine 5’-diphospho-glucuronosyltransferase (UGT2B17) gene. Pharmacogenet Genomics. 2011;21(6):325–332.
  • Zitzmann M. Mechanisms of disease: pharmacogenetics of testosterone therapy in hypogonadal men. Nat Clin Pract Urol. 2007;4(3):161–166.
  • McBride JA, Carson CC, Coward RM. Diagnosis and management of testosterone deficiency. Asian J Androl. 2015;17(2):177–186.
  • Shoskes JJ, Wilson MK, Spinner ML. Pharmacology of testosterone replacement therapy preparations. Transl Androl Urol. 2016;5(6):834–843.
  • Butler GE, Sellar RE, Walker RF, et al. Oral testosterone undecanoate in the management of delayed puberty in boys: pharmacokinetics and effects on sexual maturation and growth. J Clin Endocrinol Metab. 1992;75(1):37–44.
  • Gregory JW, Greene SA, Thompson J, et al. Effects of oral testosterone undecanoate on growth, body composition, strength and energy expenditure of adolescent boys. Clin Endocrinol (Oxf). 1992;37(3):207–213.
  • Albanese A, Kewley GD, Long A, et al. Oral treatment for constitutional delay of growth and puberty in boys: a randomised trial of an anabolic steroid or testosterone undecanoate. Arch Dis Child. 1994;71(4):315–317.
  • Brown DC, Butler GE, Kelnar CJ, et al. A double blind, placebo controlled study of the effects of low dose testosterone undecanoate on the growth of small for age, prepubertal boys. Arch Dis Child. 1995;73(2):131–135.
  • Lawaetz JG, Hagen CP, Mieritz MG, et al. Evaluation of 451 Danish boys with delayed puberty: diagnostic use of a new puberty nomogram and effects of oral testosterone therapy. J Clin Endocrinol Metab. 2015;100(4):1376–1385.
  • Chioma L, Papucci G, Fintini D, et al. Use of testosterone gel compared to intramuscular formulation for puberty induction in males with constitutional delay of growth and puberty: a preliminary study. J Endocrinol Invest. 2018;41(2):259–263.
  • Orr R, Fiatarone Singh M. The anabolic androgenic steroid oxandrolone in the treatment of wasting and catabolic disorders: review of efficacy and safety. Drugs. 2004;64(7):725–750.
  • Coviello AD, Bremner WJ, Matsumoto AM, et al. Intratesticular testosterone concentrations comparable with serum levels are not sufficient to maintain normal sperm production in men receiving a hormonal contraceptive regimen. J Androl. 2004;25(6):931–938.
  • Wu C, Kovac JR. Novel uses for the anabolic androgenic steroids nandrolone and oxandrolone in the management of male health. Curr Urol Rep. 2016;17(10):72.
  • Salehpour S, Alipour P, Razzaghy-Azar M, et al. A double-blind, placebo-controlled comparison of letrozole to oxandrolone effects upon growth and puberty of children with constitutional delay of puberty and idiopathic short stature. Horm Res Paediatr. 2010;74(6):428–435.
  • Wickman S, Dunkel L. Inhibition of P450 aromatase enhances gonadotropin secretion in early and midpubertal boys: evidence for a pituitary site of action of endogenous E. J Clin Endocrinol Metab. 2001;86(10):4887–4894.
  • Wickman S, Sipilä I, Ankarberg-Lindgren C, et al. A specific aromatase inhibitor and potential increase in adult height in boys with delayed puberty: a randomised controlled trial. Lancet. 2001;357(9270):1743–1748.
  • Rohani F, Asadi R, Mirboluk AA, et al. Letrozole effect on final height of patients with constitutional delay of growth and puberty. Med Arch. 2019;73(5):307–310.
  • Hero M, Varimo T, Raivio T. Aromatase inhibitors in puberty. Curr Opin Endocr Metab Res. 2020;14:37–41.
  • Wit JM. Should skeletal maturation be manipulated for extra height gain? Front Endocrinol (Lausanne). 2021;12:812196.
  • Boehm U, Bouloux PM, Dattani MT, et al. Expert consensus document: European consensus statement on congenital hypogonadotropic hypogonadism–pathogenesis, diagnosis and treatment. Nat Rev Endocrinol. 2015;11(9):547–564.
  • Mouritsen A, Aksglæde L, Soerensen K, et al. The pubertal transition in 179 healthy Danish children: associations between pubarche, adrenarche, gonadarche, and body composition. Eur J Endocrinol. 2013;168(2):129–136.
  • Administration UFaD. FDA briefing document for the discussion of issues related to the potential evaluation of efficacy and safety of testosterone replacement therapy in male boys with hypogonadism due to genetic or structural etiologies [FDA briefing document, pediatric advisory committee]. Rockville MD: US FDA; 2019.
  • Young J, Rey R, Couzinet B, et al. Antimüllerian hormone in patients with hypogonadotropic hypogonadism. J Clin Endocrinol Metab. 1999;84(8):2696–2699.
  • Edelsztein NY, Rey RA. Regulation of meiosis initiation in the mammalian testis: novel aspects. Curr Opin Endocr Metab Res. 2020;14:52–58.
  • Rey RA. The role of androgen signaling in male sexual development at puberty. Endocrinology. 2021;162(2):bqaa215.
  • Zacharin MR, Warne GL. Treatment of hypogonadal adolescent boys with long acting subcutaneous testosterone pellets. Arch Dis Child. 1997;76(6):495–499.
  • Pazderska A, Mamoojee Y, Artham S, et al. Safety and tolerability of one-year intramuscular testosterone regime to induce puberty in older men with CHH. Endocr Connect. 2018;7(1):133–138.
  • Young J, Xu C, Papadakis GE, et al. Clinical management of congenital hypogonadotropic hypogonadism. Endocr Rev. 2019;40(2):669–710.
  • Rey RA, Grinspon RP. Androgen treatment in adolescent males with hypogonadism. Am J Men’s Health. 2020;14(3):155798832092244.
  • Burris AS, Rodbard HW, Winters SJ, et al. Gonadotropin therapy in men with isolated hypogonadotropic hypogonadism: the response to human chorionic gonadotropin is predicted by initial testicular size. J Clin Endocrinol Metab. 1988;66(6):1144–1151.
  • Vicari E, Mongioi A, Calogero AE, et al. Therapy with human chorionic gonadotrophin alone induces spermatogenesis in men with isolated hypogonadotrophic hypogonadism–long-term follow-up. Int J Androl. 1992;15(4):320–329.
  • Zacharin M, Sabin MA, Nair VV, et al. Addition of recombinant follicle-stimulating hormone to human chorionic gonadotropin treatment in adolescents and young adults with hypogonadotropic hypogonadism promotes normal testicular growth and may promote early spermatogenesis. Fertil Steril. 2012;98(4):836–842.
  • Bouloux PM, Nieschlag E, Burger HG, et al. Induction of spermatogenesis by recombinant follicle-stimulating hormone (puregon) in hypogonadotropic azoospermic men who failed to respond to human chorionic gonadotropin alone. J Androl. 2003;24(4):604–611.
  • Sinisi AA, Esposito D, Maione L, et al. Seminal anti-Mullerian hormone level is a marker of spermatogenic response during long-term gonadotropin therapy in male hypogonadotropic hypogonadism. HumReprod. 2008;23(5):1029–1034.
  • Ulloa-Aguirre A, Lira-Albarran S. Clinical applications of gonadotropins in the male. Prog Mol Biol Transl Sci. 2016;143:121–174.
  • Lunenfeld B, Bilger W, Longobardi S, et al. The development of gonadotropins for clinical use in the treatment of infertility. Front Endocrinol (Lausanne). 2019;10:429.
  • Bougnères P, François M, Pantalone L, et al. Effects of an early postnatal treatment of hypogonadotropic hypogonadism with a continuous subcutaneous infusion of recombinant follicle-stimulating hormone and luteinizing hormone. J Clin Endocrinol Metab. 2008;93(6):2202–2205.
  • Bosch E, Nyboe Andersen A, Barri P, et al. Follicular and endocrine dose responses according to anti-Mullerian hormone levels in IVF patients treated with a novel human recombinant FSH (FE 999049). Clin Endocrinol (Oxf). 2015;83(6):902–912.
  • Fauser BC, Mannaerts BM, Devroey P, et al. Advances in recombinant DNA technology: corifollitropin alfa, a hybrid molecule with sustained follicle-stimulating activity and reduced injection frequency. Hum Reprod Update. 2009;15(3):309–321.
  • Croxtall JD, McKeage K. Corifollitropin alfa: a review of its use in controlled ovarian stimulation for assisted reproduction. Biodrugs. 2011;25(4):243–254.
  • Bistritzer T, Lunenfeld B, Passwell JH, et al. Hormonal therapy and pubertal development in boys with selective hypogonadotropic hypogonadism. Fertil Steril. 1989;52(2):302–306.
  • Liu Y, Ren XY, Peng YG, et al. Efficacy and safety of human chorionic gonadotropin combined with human menopausal gonadotropin and a gonadotropin-releasing hormone pump for male adolescents with congenital hypogonadotropic hypogonadism. Chin Med J (Engl). 2021;134(10):1152–1159.
  • Barrio R, de Luis D, Alonso M, et al. Induction of puberty with human chorionic gonadotropin and follicle-stimulating hormone in adolescent males with hypogonadotropic hypogonadism. Fertil Steril. 1999;71(2):244–248.
  • Young J, Chanson P, Salenave S, et al. Testicular anti-mullerian hormone secretion is stimulated by recombinant human FSH in patients with congenital hypogonadotropic hypogonadism. J Clin Endocrinol Metab. 2005;90(2):724–728.
  • Raivio T, Wikström AM, Dunkel L. Treatment of gonadotropin-deficient boys with recombinant human FSH: long-term observation and outcome. Eur J Endocrinol. 2007;156(1):105–111.
  • Dwyer AA, Sykiotis GP, Hayes FJ, et al. Trial of recombinant follicle-stimulating hormone pretreatment for GnRH-induced fertility in patients with congenital hypogonadotropic hypogonadism. J Clin Endocrinol Metab. 2013;98(11):E1790–5.
  • Gong C, Liu Y, Qin M, et al. Pulsatile GnRH is superior to hCG in therapeutic efficacy in adolescent boys with hypogonadotropic hypogonadodism. J Clin Endocrinol Metab. 2015;100(7):2793–2799.
  • Wei C, Long G, Zhang Y, et al. Spermatogenesis of male patients with congenital hypogonadotropic hypogonadism receiving pulsatile Gonadotropin-Releasing hormone therapy versus gonadotropin therapy: a systematic review and meta-analysis. World J Mens Health. 2021;39(4):654–665.
  • Grinspon RP, Urrutia M, Rey RA. Male central hypogonadism in paediatrics – the relevance of follicle-stimulating hormone and sertoli cell markers. Eur Endocrinol. 2018;14(2):67–71.
  • Huijben M, Lock M, de Kemp VF, et al. Clomiphene citrate for men with hypogonadism: a systematic review and meta-analysis. Andrology. 2022;10(3):451–469.
  • Chua ME, Escusa KG, Luna S, et al. Revisiting oestrogen antagonists (clomiphene or tamoxifen) as medical empiric therapy for idiopathic male infertility: a meta-analysis. Andrology. 2013;1(5):749–757.
  • Ide V, Vanderschueren D, Antonio L. Treatment of men with central hypogonadism: alternatives for testosterone replacement therapy. Int J Mol Sci. 2020;22(1):21.
  • Giagulli VA, Silvestrini A, Bruno C, et al. Is there room for SERMs or SARMs as alternative therapies for adult male hypogonadism? Int J Endocrinol. 2020;2020:9649838.
  • Bastida MG, Rey RA, Bergadá I, et al. Establishment of testicular endocrine function impairment during childhood and puberty in boys with Klinefelter syndrome. Clin Endocrinol (Oxf). 2007;67(6):863–870.
  • Stancampiano MR, Lucas-Herald AK, Bryce J, et al. Testosterone therapy and its monitoring in adolescent boys with hypogonadism: results of an international survey from the I-DSD registry. Sex Dev. 2021;15(4):236–243.
  • Grinspon RP, Gottlieb S, Bedecarras P, et al. Anti-Müllerian hormone and testicular function in prepubertal boys with cryptorchidism. Front Endocrinol (Lausanne). 2018;9:182; 1–14.
  • Grinspon RP, Arozarena M, Prada S, et al. Safety of standardised treatments for haematologic malignancies as regards to testicular endocrine function in children and teenagers. Hum Reprod. 2019;34(12):2480–2494.

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