The importance of testicular hormones in men

Some effects of the removal of testicular hormones have been implicitly known for thousands of years. Starting at an unknown period of remote antiquity, castrated men, eunuchs, were used as servants in harems and as chamberlains to kings (Humana, 1973). The fact that eunuchs were preferred for employment as guards of and servants to women may suggest that already in these ancient times it was known that castrated men had reduced or no sexual interest. There are many anecdotes about preserved sexual behaviors in some eunuchs, but these anecdotes do not contradict the proposal that most of them showed no or much reduced sexual activity. Although none of the stories concerning sexual exploits of eunuchs is based on actual observation, it is not inconceivable that some men castrated after puberty retained some sexual activity for considerable periods of time. Furthermore, some eunuchs were not castrated in the contemporary sense of the word, extirpation of the testicles, but by alternative procedures such as crushing the testicles. This may well have led to sterility, but it is not certain or even likely that hormone production was eliminated. Such cases may be those figuring in the anecdotes, at least in many of them.

It appears that some eunuchs made brilliant careers and, during the Chou period in China (1122-221 BC), many castrated men worked as advisers to the emperors. It is said that some of them were so influential that they in reality were the rulers of the Chinese empire during certain periods of the Han, T'ang, Ming and Sung dynasties (Carlson, 1972). Likewise, eunuchs were employed as public officials in the Persian empire and much later in the Roman and Ottoman empires. The impressive political success of some eunuchs suggests that castration may have many beneficial consequences. This was made still more evident during the early Christian period. A passage from the new testament, Matthew 19:12, reads:

For there are some eunuchs, which were so born from their mother's womb: and there are some eunuchs, which were made eunuchs of men: and there be eunuchs, which have made themselves eunuchs for the kingdom of heaven's sake. He that is able to receive it, let him receive it.

These words inspired many Christian men to consider castration as a means of facilitating entry into Paradise. For example, one of the great thinkers of the Greek church, Origen (complete name Oregenes Adamantius, born in 185 in Alexandria, Egypt and died in 254 in Tyre, Phoenicia) is said to have castrated himself with the purpose of avoiding sexual temptations. There was even a eunuch sect, the Valesii, active in the 3rd century, in which the members not only castrated themselves to the greater glory of God, but they also castrated any visitor to their monastery (see Kuefler, 2001 and Scholten, 1995 for more extensive discussions of eunuchs in antiquity). Again, the purpose was to reduce or eliminate the sexual urges and the sinful acts that these urges might have incited men to engage in. This means that the reduction in sexual activity following castration must have been known for more than a thousand years. Some other effects of products emanating from the testicles have also been known for a long time. In Italy, young boys were castrated in order to avoid the deepening of the voice associated with puberty. As adults, these men had a beautiful soprano voice, much appreciated by many music lovers. The practice of castration for the purpose of preserving a childish voice was discontinued by Pope Leo XIII in 1878. Here we find an example showing that some of the peripheral effects of testicular products were as well known as their central nervous effects.

The stories about eunuchs and castrati singers are certainly entertaining and stimulate our fantasies, but their value as evidence for the hypothesis that human male sexual behavior is dependent on testicular hormones is slight. Fortunately, there are many scientifically acceptable studies of the consequences of castration in men. Most, if not all, of them can be criticized because of the employment of non-representative samples, but this criticism may not be devastating. For easily understandable reasons, it is not possible to castrate a random sample of men. The men that were castrated had almost always been convicted of sexual crimes and they were normally offered a penalty rebate if they accepted castration. This practice was considered inhumane in many societies and castration is almost never performed anymore. In Norway, the procedure may still be legally performed after demand by the individual and approval by a committee, but no demand for castration has been presented since 1974. The situation is probably similar in many other countries. During the first half of the last century, though, castration of sexual offenders was regularly performed in Europe and some scientists profited from this to evaluate sexual behavior in these long-term castrates. It should be noted that all these castrations were performed post-pubertally. Thus, we do not know what the effects of prepubertal castration might be. Data from studies of castrated men in several European countries are unequivocal in the way that they all show that the intensity of sexual behaviors, including sexual dreams and fantasies, was much reduced (e.g. Wantoch, 1935; Bremer, 1958; Sturup, 1972; Heim and Hursch, 1979; Ortmann, 1980; Heim, 1981; Wille and Beler, 1989). In addition to castrating sexual offenders, medical professionals have castrated men for other reasons. One such reason is prostate cancer. Sexual behaviors are reduced or eliminated as a consequence (Bergman et al., 1984). A most interesting study in castrated cancer patients evaluated the genital response to sexual incentives in the form of a pornographic movie. Rather than relying on questionnaire or interview data like the vast majority of studies performed on castrated men, this exceptional study employed an objective measure of genital response. Penile circumference was monitored using strain gauges placed at the penile base and close to the corona. While, as mentioned in a previous chapter, pornographic movies reliably increase penile circumference in most men, only 25% of the castrated cancer patients displayed this response to the movie. Still more interesting was the observation that the men who did show erection, manifested as increased penile circumference, had serum free testosterone concentrations about double of those not displaying erection (Greenstein et al., 1995). This very important result suggests that adrenal androgen secretion may be sufficiently high, in some men, for maintaining some level of sexual functioning even in the absence of testicular androgens. It may be remembered that the only androgen source in castrated men is the adrenal gland. These data also constitute one of the very few existing pieces of direct evidence showing that the impact of sexual incentives is androgen-dependent in the human male.

The preceding brief review of sexual behaviors in castrated men should have made it evident that androgens indeed are important for these behaviors. This conclusion is somewhat obscured by two complications. One is that sexual offenders and prostate cancer patients are not necessarily representative of the general population of healthy men. The other is that humans produce androgens in the adrenal cortex. As we saw in the excellent Greenstein et al. (1995) study, this androgen production may contribute to the maintenance of sexual behaviors. Castration of the human male, as of other primates, does not reduce androgen availability as much as castration of rats and perhaps other rodents does. In contrast to primates, the rat adrenal cortex does not produce androgens (van Weerden et al., 1992) and blood androgen concentrations rapidly fall below detection limits in male rats, something that does not occur in men (BĂ©langer et al., 1989). Thus, there is no a priori reason to predict that the effects of castration on male sexual behaviors should be identical in humans and in rats. In fact, considering the difference in androgen availability after castration, its effects on sexual behaviors are remarkably similar in rats and men.

Nowadays, castration has been replaced by more sophisticated means to eliminate androgen actions. The most interesting for our purpose is the use of androgen receptor antagonists. One, cyproterone acetate, has been given both to sexual offenders and to prostate cancer patients. Results of the evaluation of sexual functioning in men being treated with cyproterone coincide nicely with those obtained in studies on castrated men. A clear-cut reduction in the intensity of all indicators of sexual behaviors was observed (Tennent, 1984; Bradford and Pawlak, 1993; Bradford and Pawlaka, 1993; Reilly et al., 2000). These data convincingly show that blockade of androgen receptors leads to serious impairment of sex behaviors in men. The significance of this observation will become evident when we analyze the role of androgen receptors in non-human males.

Another androgen receptor antagonist, flutamide, has been compared to cypro-terone in a large clinical study in prostate cancer patients. After about 6 months of treatment, spontaneous erections had declined and after about 1 year the same had happened to sexual activity. After 2 years of treatment, sexual activity had disappeared altogether in more than 80% of the patients. These data are suggestive, but the patients were rather old (with a mean of 71 years) at the beginning of the study and a substantial decline in sexual activity is not uncommon at this age (Beutel et al., 2006). The employment of a control group would have been extremely useful, but since the purpose of the study was to compare cyproterone acetate with flutamide it was not considered necessary. By the way, the antagonists did not differ with regard to their effects on sexual functioning.

Another approach that can be employed to reduce the actions of androgens is to diminish their availability by pharmacological means. While castration appears repugnant to many humans, non-surgical procedures with the same effect seem to be entirely acceptable. One efficient way to diminish blood androgen concentrations by chemical means is to administer drugs impeding gonadotrophin secretion. Strangely enough, both gonadotrophin releasing hormone (GnRH) agonists and antagonists can be used to achieve the same end. The antagonists block the actions of gonadotrophins in the testicles, while the agonists exhaust pituitary gonadotrophin reserves by a poorly understood mechanism. Both treatments have the same end result in the form of a much reduced blood concentration of androgens. The effects of such treatments are very similar to those of castration, both in sex offenders (Thibaut et al, 1993; Briken et al., 2000, 2003; Krueger and Kaplan, 2001) and in healthy young men (Bagatell et al., 1994). I will not pursue this issue any further, because I consider the evidence in favor for a considerable if not complete hormone-dependency of human male sexual behaviors convincing beyond reasonable doubt.

Before turning to studies of non-human mammals, I cannot resist the temptation to make an irrelevant comment about semantics. Treatment with androgen receptor antagonists and with drugs impeding gonadotrophin actions is called chemical castration in the popular press and some less popular outlets for written materials. On the contrary, castration is called surgical castration. Traditionally, the noun castration refers to the removing of the testicles. Thus, the expression surgical castration has no sense since surgery, in one form or another, is the only possible procedure for the removal of the testicles. Except, of course, chemical castration. This expression evokes immediately the though of some intricate procedure by which a testicle-dissolving chemical is introduced into the scrotum, leaving an empty but uncut pouch behind.

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