Taenia crassiceps infection disrupts estrous cycle and reproductive behavior in BALB/c female mice

Abstract

Previously, it has been shown that parasitic infections are able to alter the normal mammal physiology, at several extents. Thus, we investigated the effects on estrous cycle and sexual behavior induced by intraperitoneal infection with Taenia crassiceps in female host mice. Along the weeks of infection, parasites were collected from the peritoneal cavity of female mice, showing the maximum parasite load at 16 weeks. No parasites were found outside peritoneal cavity. Vaginal estrous cycle was monitored daily for 4, 8, 12 and 16 weeks of infection, and results compared against age-matched female mice. Female sexual behavior (FSB) tests were performed, one test per week. Immediately after the last behavioral test, blood was collected by cardiac puncture for steroid determinations. First of all, there was a strong tissular damage in the female reproductive tract in all infected females. The phases of the estrous cycle were interrupted at 12 and 16 weeks, with increased leukocytes and the presence of a few cornified epithelial cells and nucleated epithelial cells. The FSB decreased starting 6 weeks post infection. On the 16th week, all infected female mice ceased to exhibit sexual responses, and estradiol levels showed a significant decrease. Control mice continued showing FSB and the different phases of the estrous cycle throughout the observation period. Our results strength the notion that parasites may be considered as an evolutionary force in the reproductive ability of mammals.

Introduction

Vertebrates exhibit great diversity in reproductive strategies. Although the evolution of vertebrate reproduction has been attributed to factors such as topography (Urban et al., 2008), unpredictable larval environments (Browne and Zippel, 2007), and predation (Bonenfant et al., 2007), selective pressure from parasites must also be considered (Todd, 2007, Kokko et al., 2008). Importantly, sometimes authors ignore parasites, either unicellular or multicellular, as selective agents capable of influencing vertebrate evolution (Lampert and Schartl, 2008, Touchon and Warkentin, 2008).

Most of the reports regarding the effect of parasitic infections on estrous cycling of several host species, were done mainly in protozoan infections (Akingbade, 1992, Heinonen et al., 1988, Elhassan et al., 1994), either natural or experimental, and concluded that cycling was disrupted as a result of interference with the endocrine control system. For instance, it has been shown that, in acute malaria, the sexual physiology of the female is strongly affected (Akingbade, 1992). In another related study, infection with Trypanosoma evansi impaired estrous activity in one Friesian Holstein heifer (Payne et al., 1993). An association between weight loss and disruption of ovarian activity has been well established in dairy cows (Heinonen et al., 1988) and infection of West African Dwarf ewes with Trypanosoma vivax leads to a decrease in plasma progesterone serum levels until either recovery or death (Elhassan et al., 1994). Moreover, infection with Trypanosoma congolense induced changes in the length of estrous cycles, plasma progesterone and estradiol-17 beta levels in infected East African goats (Mutayoba et al., 1988). Furthermore, the alterations of the vaginal estrous cycle during the patent period of malaria in mice appeared as an increase in the occurrence and duration of the estrous phases. Akingbade (1992), showed a global and progressive increase in the blood concentration of estrogens and progesterone following the proliferation of Plasmodium berghei in mice.

Indeed, in rodents the cornification and desquamation of the vaginal epithelium characterizing estrus are triggered by a brief and massive increase of estrogen and progesterone release (Norris and Adams, 1981). Particularly in the case of female Taenia crassiceps infected mice, no morphological or histological modifications were found in the clitoral glands as a consequence of the infection (Gourbal and Gabrion, 2006).

Our hypothesis is that Taenia crassiceps will disrupt estrous cycle, due to the fact that it has been previously demonstrated that infection with this parasite, induce strong hormonal changes in its host. Since little is known of the effects of T. crassiceps on the reproductive ability of its female host, and due to the fact that there are very few reports in the literature that have determined that helminth parasites can alter normal female physiology, the aim of this study was to assess the effects of the infection upon the sexual behavior, estrous cycle and hormonal changes in female BALB/c AnN mice and to correlate these parameters with parasite intensity in the host. Our results demonstrate that there is a disruption of the normal estrous cycle in infected female mice and, as a consequence, there is complete inhibition of FSB. This suggests novel forms of affecting the evolution of both host and parasite in addition to prey/predator interactions, and strength the notion that parasites may be considered as an evolutionary force in the reproductive ability of mammals.