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Update on Male Hormonal Contraception: Is the Vasectomy in Jeopardy?

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Update on Male Hormonal Contraception: Is the Vasectomy in Jeopardy? International Journal of Impotence Research (2010) 22, 159–170 & 2010 Nature Publishing Group All rights reserved 0955-9930/10 $32.00 www.nature.com/ijir REVIEW Update on Male Hormonal Contraception: Is the Vasectomy in Jeopardy? GJ Manetti1 and SC Honig1,2,3 1Division of Urology, Yale-New Haven Hospital, New Haven, CT, USA; 2Division of Urology, Hospital of Saint Raphael, New Haven, CT, USA and 3Division of Urology, University of Connecticut, Farmington, CT, USA Traditionally, male contraception has consisted of either barrier methods, such as condoms, or vasectomy. However, in recent years, we have made great strides in the basic science and clinical medicine to better understand the feedback mechanisms and physiology of the male reproductive system. These advances have enabled the development of several nonsurgical, hormonal, reversible, well-tolerated alternatives for male contraception. Men are more likely now than ever to participate in the choice of contraceptive techniques. This review will discuss the current status and recent developments in nonsurgical hormonal male contraception, a field that has been historically limited by social, financial and physiological challenges. International Journal of Impotence Research (2010) 22, 159–170; doi:10.1038/ijir.2010.2; published online 25 March 2010 Keywords: contraception; testosterone; sperm; male infertility; spermatogenesis Update on male hormonal contraception: study involving 450 women also suggested that is the vasectomy in jeopardy? women would both trust and welcome their male partner to take a more active role in contraception.3 Male contraception has traditionally consisted of Approximately half of all conceptions are un- either barrier methods, such as condoms or vasect- planned, resulting in unintended pregnancies and 4 omy. Vasectomy is a permanent, expensive, surgical subsequent elective terminations. Therefore, it has solution with very low failure rates of 1/2000.1 become quite important to develop less invasive, Condoms are a less desirable option and with more tolerable and more reversible methods of male typical and ideal use results in a 14 and 3% yearly contraception that have a success rate similar or pregnancy rate, respectively. The ideal contracep- better than female hormonal contraception. This tive would be 100% effective, reversible, noninva- review will discuss the current status and recent sive, affordable, with no short- or long-term side developments in male contraception, a field that has effects. been historically limited by social, financial and Men are more likely now than ever to participate physiological challenges. in the choice of contraceptive techniques, although there are notable variations between population groups and cultures.2 Furthermore, an international Review of hypothalamic–pituitary– gonadal axis and spermatogenesis Correspondence: Dr SC Honig, Department of Urology, University of Connecticut, 330 Orchard Street, Suite 164, An understanding of the endocrinology of male New Haven, CT 06511, USA. reproduction, specifically the male hypothalamic– E-mail: [email protected] pituitary–gonadal axis and the basics of spermato- This article has drawn upon material from Honig SC and genesis is required to understand the methodologies Sandlow J. Male contraception and vasectomy. In: Lip- used for male contraception. shultz L, Howards SS, Niederberger CS (eds). Infertility The hypothalamic–pituitary–gonadal pathway is in the Male, 4th edn. Cambridge University Press: Cam- bridge, UK, 2009, pp 474–492, reproduced with permis- regulated through negative feedback by downstream sion. products as summarized in Figure 1. Spermatogen- Received 3 November 2009; revised 23 December 2009; esis is regulated by the pulsatile release of gonado- accepted 24 December 2009; published online 25 March tropin-releasing hormone (GnRH) from the arcuate 2010 nucleus of the hypothalamus, which stimulates the Update on male hormonal contraception GJ Manetti and SC Honig 160 tially be another indirect target to suppress sperma- togenesis. However, the role of inhibin in FSH suppression and spermatogenesis is unclear, as low levels of inhibin are still present with LH-receptor mutations and chronic FSH administration.8,10,11 Progesterone receptors are seen in the hypothala- mus, pituitary and testis. It appears that progester- one affects gonadotropins via the hypothalamic– pituitary–testis axis, however, they may function directly on the testis as well.12,13 It is clear that in normal sperm-producing men, intratesticular testosterone levels are 100-fold higher than in serum.14–18 Interestingly, LH-receptor-defi- cient mice can support some level of spermatogen- esis, but use of an androgen receptor antagonist such as flutamide will suppress spermatogenesis com- pletely.19–21 The role of dihydrotestosterone, a potent metabolite of testosterone, in spermatogen- Figure 1 Endocrinology of spermatogenesis. The hypothalamic– esis appears to be less clear. A decrease in pituitary–gonadal axis. dihydrotestosterone levels does not seem to cause a significant drop in sperm production.22 anterior pituitary to episodically release follicle- On a cellular and receptor level, androgen stimulating hormone (FSH) and luteinizing hor- receptors are found in multiple cell sites within mone (LH). LH stimulates the Leydig cells to the testes, specifically immature germ cells, smooth produce testosterone, which has a local effect on muscle cells, myoid cells, Sertoli and Leydig cells. the interstitium and seminiferous tubules and Cell-specific effects on androgen receptors may results in sperm production and maturation. This affect spermatogenesis. In Sertoli cell and Leydig effect is manifested by very high intratesticular cell androgen receptor-specific knockout mice, testosterone compared with the bloodstream. FSH spermatogenesis is impaired.23–26 In contrast, an- exerts its effect directly on the Sertoli cells to drogen receptors on germ cells and myoid cells promote spermatogenesis. Testosterone and estra- appears to be less important in spermatogenesis as diol (converted through aromatase in the testis knock out models in these situations, do not impair interstitium) are direct negative feedback modula- spermatogenesis in a major way.23,27 Compounds tors of GnRH, LH and FSH. Aromatase inhibition that are cell specific and influence Sertoli and increases FSH levels suggesting that FSH regulation Leydig cell androgen receptors could potentially be is more dependent on estradiol than testosterone.5,6 an excellent site of future male contraceptive Other substances have a role in this important thoughts. As described earlier, complete blockage neuroendocrine negative feedback pathway. Studies of the androgen receptor with flutamide suppresses have shown that kisspeptins, a group of amino-acid spermatogenesis.28 Molecules that follow this path- peptides, and their G-protein-coupled receptor way, but may be more specific and do not have the (GPR54) have a critical function in the secretion of significant negative side effects of flutamide, may be GnRH and the negative feedback of testosterone and valuable potential contraceptive targets. estradiol on the hypothalamus. Administration of Spermatogenesis is hormone dependent. Sperma- kisspeptin has been shown to increase GnRH togonia divide in 16-day intervals to form B secretion in neuronal cell lines.7 Furthermore, spermatogonia, which will differentiate and pro- although acute administration of kisspeptin seems gress through spermatogenesis. Other B spermato- to increase LH, FSH and testosterone secretion, gonia will renew to form new precursor stem cells. chronic administration lowers serum LH levels in Type B spermatogonia that differentiate will divide monkeys.8,9 Manipulation of the kisspeptin–GPR54 mitotically to form primary spermatocytes and these pathway represents another potential target for will undergo meiosis to secondary spermatocytes future male contraceptive therapy.8 and round spermatids. The round spermatids will Complex interplay between testosterone, FSH and then undergo a process of conformational change other factors is important for normal spermatogen- into mature spermatids. In this process, they will esis. Sertoli cells are part of the seminiferous tubules undergo extensive changes in cytoplasm and nu- that are activated by FSH and function to provide cleus, form an acrosome, flagellum and cytoplasmic the optimal environment for the developing sperm organelles undergo changes to form a mature cells throughout spermatogenesis. Inhibin B repre- spermatozooan. This process requires approxi- sents a nonsteroidal substance released by Sertoli mately 64 days. High levels of intratesticular cells after puberty and functions as a negative testosterone are required for this to occur. Hypo- feedback on FSH secretion. Inhibin B could poten- physectomy results in testis atrophy, but not International Journal of Impotence Research Update on male hormonal contraception GJ Manetti and SC Honig 161 Table 1 Male hormonal contraceptive options contraception by 20 years. In 1939, two investigators independently tested testosterone for suppression of Testosterone spermatogenesis.33,34 Since then, female birth con- Testosterone propionate Testosterone enanthate trol pills have dominated the contraceptive market. Testosterone undecanoate It has been difficult to equal or improve on the Testosterone buciclate safety, efficacy and reversibility of female birth 7a-methyl-19-nortestosterone control pills, as the bar has
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