Cysticercus tenuicollis Vesicle in Fetal Structures: Report of a Case

Introduction

Cysticercus tenuicollis is the metacestode of the tapeworm Taenia hydatigena. Adult worms have been reported to have been found in the small intestines of dogs, cats, mice and wild carnivores, like the wolf and the fox (Euzéby 1966; Soulsby 1988). Infected carnivores eliminate T. hydatigena eggs with their faeces. Herbivores become infected with the eggs on account of having fed on contaminated pastures. Possible intermediate hosts for C. tenuicollis are squirrels, cattle, sheep, goats and other wild ruminants and also swines. After ingestion, the egg’s shell is digested and the oncospheres become free to migrate through the intestinal walls, reaching the liver through the hepatic portal system. The oncospheres may remain in the liver or migrate to the omenta, the mesenteries and the serosal surface of the peritoneal cavity, where they attach and initiate post-oncospheral development (Euzéby 1966; Soulsby 1988; Sanchez Acedo 1999).

The prevalence of the C. tenuicollis infection varies according to the geographical areas and generally reaches higher incidences in countries with a lower degree of sanitary control and with an uncontrolled wild carnivore population (Sanchez Acedo 1999; Budka et al. 2004). Infection of small ruminants with cysticerci of T. hydatigena is frequently not significant, and most of the times a diagnosis is made at the abattoir. However, the effect of this infection upon the hosts depends largely on the degree of the parasitism, the organs involved and the existence of other concurrent infections (Sanchez Acedo 1999).

The most frequent locations for C. tenuicollis are the omenta, the mesenteries or the liver. However, unusual locations of cysticerci of T. hydatigena, like the lungs, the kidneys and the brain, have also been reported (Euzéby 1966; Sanchez Acedo 1999). The existence of C. tenuicollis cysts attached to the broad ligament and to the uterine tubes was reported in an abattoir survey on acquired reproductive abnormalities in the ewes. In a certain number of these cases (3 : 10), calcified cysticerci occluded the uterine tubes (Smith et al. 1999).

To the authors’ best of knowledge, this is the first report on the finding of a viable C. tenuicollis vesicle inside the fetal structures.

Case report

In the case presented here a C. tenuicollis vesicle was found inside of the fetal allantoic cavity, adjacent to the amniotic membrane of one of the foetuses in a gemelliparous pregnant goat uterus.

The pregnant uterus of a 3-year-old goat (Capra hircus) was obtained following its necropsy and thereafter dissected for teaching purposes. It was a uterus with a gemellar gestation of around 70 days. The goat was part of a 40-animal-flock, raised under the traditional management system of Portugal’s Northeast. During the daylight, the animals were allowed to graze on natural pastures, either private or communal, and at night they were lodged. Generally, besides the pasture no other supplements were given. The deworming of the flock was performed once a year with Ivermectin (Oramec^®; Merial Portuguesa, Rio de Mouro, Portugal) by local official agencies, concomitant with other sanitary interventions. The deworming of the sheep–dogs was under the owner’s responsibility, and was not regularly carried out. This animal was culled due to progressive emaciation and the necropsy was requested to ascertain the existence of a parasitic or an infectious cause of disease.

According to the animal’s necropsy report, the existence of pulmonary abscesses and two small-sized cysticerci vesicles (around 2 cm in diameter) in the peritoneal cavity was observed. The appearance of the uterus was normal, with similar distention of the uterine horns consistent with a gemellar pregnancy. During the dissection procedures, after the uterine wall and the fetal chorion had been incised, a viable parasitic vesicle was observed inside the allantoic cavity of one of the foetuses (Fig. 1a). A closer observation revealed the existence of a cystic structure, 6 cm in diameter, containing a colourless fluid enclosed by a thin membrane and showing cephalic invagination with a single scolex. Posterior assessment of the cysticercus’ morphology allowed its identification as C. tenuicollis (Euzéby 1966; Soulsby 1988). The parasitic vesicle integrity allowed its morphological classification and consequently no further procedures were attempted.

The Cysticercus was located parallel to the amnions, without signs of fusion between its cover and the fetal membranes. Macroscopic signs of inflammation were not visible. The necropsy of the foetus did not reveal the existence of any additional cysticerci.

The placentomes located nearest to the cysticercus showed two to three times greater development than equivalent placentomes in the contralateral gestation. They also evidenced a brownish colouration when compared to the adjoining placentomes (Fig. 1b), which gave them a necrotic appearance.

For histopathological examinations, samples of the uterus and fetal membranes in the area surrounding the cysticercus were collected and fixed in 10 per cent buffered formalin and processed according to the standard histological techniques for paraffin embedding. Tissue sections 2-μm thick were done and used for conventional haematoxylin–eosin (H–E) staining. To evaluate the existence of any ferric pigment, a Prussian blue staining was also performed. Normal cotyledonal areas of the uterus and fetal membranes were also collected on the contralateral uterine horn to serve as controls, and were processed as above.

Histopathological analysis of the cotyledones surrounding the cysticercus revealed the existence of some necrosis of the epithelia and the uterine wall. Signs of active inflammation were absent. Sporadic macrophages containing a brownish cytoplasmatic pigment with a granular pattern were observed in the connective tissue of placentomes adjoining the cysticercus. This pigment was negative to ferric pigment staining. Neither granulomatous reactions, eosinophilic infiltrates etc., were observed around the bladder wall of the parasite, nor the cysticercus presented signs of degeneration.

The presence of a cysticercus vesicle inside of the fetal allantoic cavity leads us to presume that it derived from an oncosphere that was carried in the blood supply to the uterus. From a small capillary of the cotyledonal region, it probably migrated through the placental barrier reaching the vascular network of the allantoids, and then accessing the allantoic cavity. This would be possible on account of the cytolytic activity of the oncosphere (Heath 1971; Cheng 1986).

The uterine structures revealed a discrete inflammatory reaction in the placentomes adjoining the cysticercus. It is generally accepted that, in order to survive, oncospheres and cysticerci from other Taenia are able to evade the host immune system, either by using a passive escape technique or through immunomodulation (Terrazas et al. 1998; Molinari et al. 2000; Pérez-Torres et al. 2002). It is also true that viable cysticerci of other Taenia are surrounded by a limited inflammatory reaction and that the death of the parasite leads to an intense inflammatory reaction (Chi and Chi 1978; Sanchez Acedo 1999). Besides, the presence of the cysticercus inside the placenta makes it easier to bypass the local immunological system. Furthermore, during gestation, an increment in allantoic fluid osmolality and electrolyte concentrations is observed (Faichney et al. 2004). Water and solutes that were part of the allantoic fluid may have accounted for the growth of this cysticercus.

In the ewe, viable and degenerative cysts have been observed in the ovaries, uterine tubes, uterus, cervix and vagina (Sanchez Acedo 1999; Smith et al. 1999). Nevertheless, to the best of the authors’ knowledge, this is the first report that documents the existence of a C. tenuicollis vesicle inside of the fetal membranes. Apparently, its presence did not compromise the normal development of the fetus that carried this cysticercus. Moreover, the finding of a C. tenuicollis vesicle behind the placental barrier alert for the possibility of oncosphere migrations into the developing fetus in pregnant females.