Acta Tropica 109 (2009) 141–145
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Acta Tropica
journal homepage: www.elsevier.com/locate/actatropica
Taenia crassiceps infection disrupts estrous cycle and reproductive behavior in
BALB/c female mice
Marcela Arteaga-Silva
a
, José Antonio Vargas-Villavicencio
b
, Rosa María Vigueras-Villase˜ nor
c
,
Mauricio Rodríguez-Dorantes
b
, Jorge Morales-Montor
b,∗
a
Departamento de Biología de la Reproducción, Universidad Autónoma Metropolitana, Iztapalapa, A.P. 55 535, México, D.F. 09340, Mexico
b
Departamento de Inmunología, Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México, A.P. 70228, México, D.F. 04510, Mexico
c
Laboratorio de Histomorfología, Instituto Nacional de Pediatría, México, D.F., Mexico
article info
Article history:
Received 4 April 2008
Received in revised form 21 June 2008
Accepted 17 October 2008
Available online 8 November 2008
Keywords:
Cysticercosis
Taenia crassiceps
Parasite
Infection
Sexual behavior
Estrous cycle
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.
© 2008 Elsevier B.V. All rights reserved.
1. 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). Impor-
tantly, 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 proto-
zoan infections (Akingbade, 1992; Heinonen et al., 1988; Elhassan
et al., 1994), either natural or experimental, and concluded that
∗
Corresponding author. Tel.: +52 55 56223854; fax: +52 55 56223369.
E-mail addresses: jmontor66@biomedicas.unam.mx, jmontor66@hotmail.com
(J. Morales-Montor).
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 Try-
panosoma 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 proges-
terone 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
0001-706X/$ – see front matter © 2008 Elsevier B.V. All rights reserved.
doi:10.1016/j.actatropica.2008.10.011