First case of peritoneal cysticercosis in a non-human primate host (Macaca tonkeana) due to Taenia martis
© Brunet et al.; licensee BioMed Central Ltd. 2014
Received: 17 April 2014
Accepted: 22 August 2014
Published: 4 September 2014
Infections with larval stages (metacestodes) of a variety of taeniid species have been described in primates, including humans, with partial to severe clinical consequences. Taenia martis is a tapeworm of mustelids, and martens are mainly their definitive hosts in Central Europe. In the rodent intermediate host cysticerci develop in the pleural and peritoneal cavities. The present report describes a case of T. martis peritoneal cysticercosis in a Tonkean macaque.
An abdominal mass was detected in a 3-year-old male Tonkean macaque (Macaca tonkeana) born and raised in a primate colony in France. Examination of the mass after laparotomy showed numerous vesicles identified as cysticerci of T. martis, based on the morphology of scolex and hooks, with confirmation by PCR amplification and sequence analysis of the mitochondrial cytochrome c oxidase subunit 1 (cox1) and NADH dehydrogenase subunit 1 (nad1) genes. Exeresis of the lesion was not possible and praziquantel (5.7 mg/kg) was given twice at an interval of 3 days. The abdominal mass was greatly diminished upon examination 2 months later and no signs of recurrence were noticed during the following 4 years.
This is the first report of T. martis cysticercosis in a monkey. This record and the recent first description of an ocular T. martis cysticercosis in a human show the susceptibility of primates to T. martis and its zoonotic potential. This taeniid species must be considered in the differential diagnosis of cysticercosis in primates.
Non-human primates might act as aberrant hosts for a number of cestode species after peroral infection and larval development in extra-intestinal locations can have potentially severe clinical consequences [1–6]. In most cases the circumstances of infection of captive monkeys remains unclear . Tonkean macaques (Macaca tonkeana, Cercopithecidae) are housed in social groups in large enclosures, and are often used for ethological research . Taenia martis (Zeder, 1803) is a tapeworm that develops in the small intestine of wild carnivores (Mustelidae). In Europe it is commonly found in Martes foina, the stone marten, and in M. martes, the pine marten. Other mustelids, and more rarely canids, might also act as definitive hosts . The stone marten is established in the Northern Hemisphere and is widely found in France with the highest population densities reported in eastern regions . T. martis has been observed in martens in Italy, Germany and Switzerland [10, 11] but there is a lack of information concerning its distributional range in France. However, cestodes found in Martes foina near Nancy and Paris, which were originally described as T. intermedia (Rudolphi, 1809), were later classified as T. m. martis[12, 13]. T. martis is maintained in a wild-animal cycle between carnivores and small rodents which act as intermediate hosts, mainly Myodes voles and Apodemus field mice. In Europe, prevalences of T. martis larvae in different rodents have been reported to vary between 0.95% in bank voles (Clethrionomys [currently Myodes] glareolus) in the French Pyrenees, 2% in Apodemus flavicollis in Switzerland, and 22% in musk rats (Ondatra zibethicus) in Belgium [11, 14, 15]. Recently, a first case of cysticercosis due to T. martis was observed in a human patient in Germany that shows the zoonotic potential of this cestode species . The susceptibility of primates to T. martis infection is also supported by the present case of a peritoneal cysticercosis due to T. martis in a Tonkean macaque that, to the best of our knowledge, had never been reported before in a non-human primate.
In the present case, the completion of the cestode life-cycle is highly probable in the environment of the park as small rodents and carnivores including martens were regularly observed in the close vicinity. The infection of the monkey was likely through ingestion of taeniid eggs during foraging activities, which are quite developed in Tonkean macaques . Taeniid eggs might contaminate soil and grass when scattered by rain from faeces of wild carnivores, which are often found near the fences or possibly inside the enclosure as access of martens to this wooded park is not excluded. Direct infection by picking the potentially contaminated faeces, especially when they contain fruit stones or during grooming from the fur of monkeys from the ground, are other hypotheses. In our case, clinical evolution was quite favourable. Although praziquantel had demonstrated a variable efficacy in the treatment of metacestodoses [17, 24], this cestodicidal drug was chosen because its injectable administration to the macaque was easier and more reliable than fenbendazole or albendazole, which would have required daily oral administration for several weeks. The localized infection observed in this macaque and the complete cure without surgical resection could be explained by a high sensitivity of T. martis larvae to praziquantel, by adequate host defenses (as no sign of immunosuppression was observed in the animal), and also by the absence of proliferation of the parasites. Indeed, the fully-developed cysticerci of T. martis are non-multiplying larvae contrary to those of T. crassiceps which proliferate by budding [8, 17, 25]. In the case of T. martis metacestodosis reported recently in an immunocompetent woman in southeastern Germany, the lesion was due to a single cyst localized in the eye and the cure was obtained by surgical removal of the parasite . The present report shows the susceptibility of macaque to T. martis larvae and indicates the occurrence of an environmental contamination with T. martis eggs. It highlights the potential risk of infection for captive monkeys and also for humans with this taeniid species, which should be considered in the etiology of atypical cysticercosis cases.
We thank Dr Bruno Polack from the Ecole Nationale Vétérinaire d’Alfort for technical assistance with some photographs. We thank Dr. Holly Tuten for editing the manuscript. We would like to thank Dr Bruno Mathieu for establishing the neighbour-joining tree.
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