Elsevier

Physiology & Behavior

Volume 75, Issue 5, 15 April 2002, Pages 689-696
Physiology & Behavior

Developmental exposure to polychlorinated biphenyls affects sexual behavior of rats

https://doi.org/10.1016/S0031-9384(02)00673-XGet rights and content

Abstract

Polychlorinated biphenyls (PCBs) are persistent environmental contaminants that have the potential to disrupt reproduction through a variety of different pathways. In the present study, we investigated the effects of fetal and lactational PCB exposure on reproductive behavior in male and female laboratory rats. These pregnant rats were injected daily with either 2,4,2′,4′-tetrachlorobiphenyl (PCB 47) at the dosage of 1 or 20 mg/kg body weight or 3,4,3′,4′-tetrachlorobiphenyl (PCB 77) at the dosage of 0.25 or 1 mg/kg body weight or sesame oil (control group) from gestational days 7 to 18. Offspring were then tested for sexual behavior as adults. Exposure to both PCB 77 and PCB 47 reduced the level of sexual receptivity in the female offspring, but had no detectable effects on the sexual behavior of the male offspring. In addition to changes in adult sexual behavior in the females, both PCBs produced a significant increase in the females' anogenital distance, suggesting a modification of androgen responsiveness in females resulting from PCB exposure during development. Similar effects were not seen with the males.

Introduction

Polychlorinated biphenyls (PCBs) are persistent environmental pollutants because of their chemical stability and ability to accumulate in the food chain. They are detected in the air, water, sediments, wildlife, and human adipose tissue, milk, and serum [1], [2], [3], [4]. PCBs have the potential to disrupt reproduction through various pathways. They are reported to decrease female fertility by reducing implanted ova and increasing the degeneration rate of embryos in mice [5], [6]. A possible mechanism for this effect is through the change of the biochemical environment of the ovaries and uterus during oogenesis or pregnancy [7], [8]. PCBs also affect male fertility by depressing the reproductive organs [9], [10] and by reducing sperm production [9]. Further, androgen metabolism was altered in males [10], [11], [12], and progesterone (P) synthesis was disrupted in female rats [13], following exposure to PCBs.

Perinatal treatment with the PCB mixtures, Aroclor 1221 and Aroclor 1254, has been shown to decrease sexual behavior in female rats [14], [15], [16]. These commercial PCB mixtures are composed of different concentrations of coplanar and noncoplanar PCBs. Therefore, some PCBs, such as the commercial mixture A1221, may act as endocrine disrupters because of their affinity for estrogen receptors [17]. However, other PCB mixtures, such as A1254, exhibit minimal binding to estrogen receptors, and some of their metabolites may even have antiestrogenic activity [4], [17]. In this study, we evaluate the effects of prenatal exposure to the dioxin-like PCB congener 3,4,3′,4′-tetrachlorobiphenyl (PCB 77), and the noncoplanar di-ortho-substituted PCB congener, 2,4,2′,4′-tetrachlorobiphenyl (PCB 47), on the development of sexual behavior in the laboratory rat. Both of these congeners have been shown to alter brain dopamine levels (see [18], [19] for review), a neurotransmitter that plays an important role in mediating male and female sexual behavior [20], [21]. PCB 77 is also reported to have estrogenic and antiestrogenic activity [22], [23].

Section snippets

Methods

Fifty time-mated Long–Evans female rats were purchased from Harlan–Sprague Dawley (Indianapolis, IN). Upon arrival, the rats were randomly divided into five groups and housed individually in plastic cages (50×25×20 cm). There was a minimum of nine dams per experimental treatment. These animals were kept in a colony room at 23±2 °C, under a 12:12 light/dark cycle (lights on at 1900 h) and with a relative humidity of 55%. Food (Harlan Teklad 22/5 rodent diet #8640, Madison, WI) and tap water were

Behavioral results

Prenatal exposure to PCB 77 decreased sexual receptivity in female rats as measured by LQ (χ2=20.365, df=2, P<.001; Fig. 1); however, treatment with PCB 47 had a significant effect only in the 20-mg/kg group (χ2=6.868, df=2, P<.05). Exposure to PCB 77 significantly decreased the AL of the females [F(2,25)=4.905, P<.05] in both the 0.25- and 1-mg/kg groups compared with that of the control group (Fig. 2). Treatment with PCB 47 did not significantly affect AL. MRL, IRL, and PER were not affected

Discussion

Our results demonstrate that prenatal exposure to both the coplanar congener PCB 77 and the ortho-chlorinated congener PCB 47 at subtoxic doses reduces sexual receptivity of female rats as measured by the LQ. This effect was seen at both doses for the coplanar PCB, but only at the relatively high dose in the case of PCB 47. All PCB-treated groups that showed deficits in lordosis also showed a significant increase in anogenital distance. Since PCB 77 has been reported to be estrogenic as well as

Acknowledgements

The work in this manuscript was supported by NIEHS Superfund Grant P42ES049 and NSF Grant IBN9728883 to Lynwood G. Clemens and by a grant from the Sichuan Provincial Education Commission, China to X.Q. Wang.

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      Sexual behavior studies in male rats showed that developmental PCB77 or PCB126 increased numbers of intromissions but did not affect pregnancy outcomes (Faqi et al., 1998). Another report in male rats reported no effect of PCB47 or PCB77 (Wang et al., 2002). By contrast, measures of sexual behavior in females have revealed effects of developmental PCB exposures.

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