Environmentallifestyle Effects On The Adult Testis That Arise During Fetal Development

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There is growing evidence that a syndrome of interconnected disorders affecting the human male, so-called testicular dysgenesis syndrome, may have a common origin in fetal life (Fig. 1) during the period of sexual differentiation (68). Manifestations of this syndrome in adulthood can include low sperm counts/reduced fertility and/or testicu-lar germ cell cancer, as well as a history of cryptorchidism and/or hypospadias (see Fig. 3); other potential aspects, such as lowered testosterone levels for life, remain to be clearly defined. Several of these disorders are increasing in incidence, with environmental/lifestyle causes implicated in this increase (68). An integral part of this syndrome of disorders is evidence for impaired hormone production/action or abnormal hormone balance (e.g., between androgens and estrogens [5,8]) during the period of sexual differentiation and fetal development (see Fig. 3). These could arise for several reasons, for example because of intrauterine growth retardation (IUGR) of the affected fetus (5,8,103) or because of exposure of the mother to an environmental chemical with intrinsic hormonal activity or ones which may alter endogenous hormone levels (5,8). For numerous reasons, it is currently difficult to evaluate these various possibilities in a definitive way, so a brief overview of the available evidence that relates to environmental/lifestyle influences is presented. Further details and discussions can be found elsewhere (3,5,8).

It is perhaps not widely recognized that male reproductive development disorders are extremely common. For example, the two most common congenital malformations in children of either sex are both male sexual differentiation disorders, namely cryp-torchidism and hypospadias, which affect 2-4% and 0.3-0.7% of boys at birth, respectively (8). This reminds us that development of the male reproductive system does not occur by default, as is largely the case in the female, but instead requires the timely production and action of hormones by the fetal testis—mainly testosterone but also anti-Mullerian hormone and insulin-like factor-3 (INSL-3) (5,8,104). Any dietary, lifestyle, or environmental exposures that act through the mother to affect general growth or timing of growth of the fetus or hormone production by the fetal testis can therefore potentially affect development of the reproductive system of the male fetus. For example, IUGR is associated with increased risk of both cryptorchidism and hypospadias (8,103,105). In turn, these disorders have important lifelong consequences in terms of risk of infertility/low sperm counts and of developing testicular germ cell cancer in adulthood (4,8,106,107) (see Fig. 3).

Maternal lifestyle can be an important determinant of IUGR and of fetal growth in general (3). Smoking by the pregnant mother has well-established effects on fetal growth, which can, in turn, alter risk of a range of disorders of the fetus when it has grown to adulthood (7)—these can include effects on fertility, but these are most obvious in female offspring (3). However, there is evidence that maternal smoking can adversely affect sperm counts of male offspring in adulthood (108). More generally, the trend to obesity in Western countries means that when these women become pregnant, there is increased risk of fetal growth problems, presumably resulting from the insulin resistance that accompanies obesity (3,7).

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