Subcutaneous Taenia crassiceps Cysticercosis in a Ring-Tailed Lemur (Lemur catta) in a Serbian Zoo.

BACKGROUND: Different rodent species serve as natural intermediate hosts for carnivore tapeworm Taenia crassiceps. However, this cestode occasionally infects various dead-end hosts including humans and other primates and may cause serious pathological implications with potentially fatal outcome. In this paper, we present subcutaneous cysticercosis caused by T. crassiceps, found in a previously healthy 17-years-old male ring-tailed lemur (Lemur catta) in a Serbian Zoo. CASE PRESENTATION: The animal was presented to a veterinarian with a history of periarticular subcutaneous swelling in medial right knee region. After fine needle aspiration revealed cycticerci-like structures, a surgery was performed for complete extraction of the incapsulated multicystic mass containing numerous cysticerci. Collected material was sent for parasitological, histological and molecular analysis. One month after surgery, the lemur died due to respiratory failure unrelated to cysticercosis. Based on morphological features of large and small hooks and characteristic proliferation of cysticerci, a metacestode of T. crassiceps was identified, which was confirmed after sequencing of obtained amplicons and comparing them to the GenBank database. CONCLUSIONS: This is one of the few reported cases of T. crassiceps cysticercosis in a ring-tailed lemur, and the first one in Serbia. This endangered species seem to be more sensitive for T. crassiceps than other non-human primates, which represents serious conservation challenge for captive animals. Due to zoonotic nature of the parasite, challenging diagnosis, severity of the disease, difficult treatment and possible fatalities, high biosecurity measures are of particular importance, especially in endemic regions.

Fatal pulmonary cysticercosis caused by Cysticercus longicollis in a captive ring-tailed lemur (Lemur catta).

Here we describe fatal pulmonary cysticercosis caused by Cysticercus longicollis, the larval stage of Taenia crassiceps in a 15-year-old female ring-tailed lemur (Lemur catta) from Sarajevo Zoo. After sudden death, the lemur was subjected to necropsy and large multicystic structure, subdivided with fibrous septa and filled with numerous translucent, oval to ellipsoid bladder-like cysts (cysticerci), almost completely replacing right lung lobe was observed. In addition, numerous free and encysted cysticerci were found in the thoracic cavity. Histopathology revealed connective tissue outlined cavities that compress lung parenchyma. Each cavity contained several thin walled cysticerci with single inverted protoscolex, one or more suckers and rostelum with two rows of hooks. In many of the cysticerci one or several exogenous buds of daughter cysticerci were observed. Based on morphology and microscopic appearance the parasite was identified as C. longicollis. Subsequent molecular analysis and sequencing confirmed presumptive diagnosis. To our knowledge, this case represents the first report of T. crassiceps and cysticercosis caused by C. longicollis in Bosnia and Herzegovina.

Fatal echinococcosis in three lemurs in the United Kingdom--A case series.

Tapeworms of the genus Echinococcus reside in the small intestine of a number of carnivorous species, predominantly canids. In enzootic areas, hydatidosis caused by taeniid metacestodes can present a significant problem in accidental intermediate hosts, including humans. Whereas the United Kingdom is currently considered free of Echinococcus multilocularis, Echinococcus granulosus sensu stricto (s.s.) and Echinococcus equinus are endemic in the UK and have been reported in a variety of captive mammals. The presentation of echinoccocosis in non-human primates widely parallels disease in humans, and public health concerns are related to the four genera, E. granulosus, E. multilocularis, Echinococcus vogeli and Echinococcus oligarthrus. In contrast, sporadic outbreaks and individual hydatid disease cases in non-human primates have been associated with several Echinococcus and Taenia species. Here we describe three fatal cases of cystic echinococcosis in two captive ring-tailed lemurs (Lemur catta) and one captive red-ruffed lemur (Varecia variegata rubra) and provide molecular tapeworm characterisation. To the best of the authors' knowledge, this includes the first report of Echinococcus ortleppi in a UK born ring-tailed lemur and provides the first in depth case reports of echinococcosis due to E. equinus in UK born ring-tailed and red ruffed lemurs with detailed clinical and pathological findings. The cestode life cycle and implications for zoo collections are discussed.

Surveillance and management of Echinococcus multilocularis in a wildlife park.

The fox tapeworm Echinococcus multilocularis is the causative agent of alveolar echinococcosis, a severe zoonotic disease that may be fatal if untreated. A broad spectrum of mammalian species may be accidentally infected even in captivity. In April 2011, liver lesions due to E. multilocularis were observed during the necropsy of a captive-born nutria (Myocastor coypus) in a French wildlife park, leading to initiation of a study to survey the parasite's presence in the park. A comparable environmental contamination with fox's feces infected by E. multilocularis was reported inside (17.8%) and outside (20.6%) the park. E. multilocularis worms were found in the intestines of three of the five roaming foxes shot in the park. Coprological analyses of potential definitive hosts in captivity (fox, lynx, wildcat, genet, wolf, bear and raccoon) revealed infection in one Eurasian wolf. Voles trapped inside the park also had a high prevalence of 5.3%. After diagnosis of alveolar echinococcosis in a Lemur catta during necropsy, four other cases in L. catta were detected by a combination of ultrasound and serology. These animals were treated twice daily with albendazole. The systematic massive metacestode development and numerous protoscoleces in L. catta confirmed their particular sensitivity to E. multilocularis infection. The autochthonous origin of the infection in all the captive animals infected was genetically confirmed by EmsB microsatellite analysis. Preventive measures were implemented to avoid the presence of roaming foxes, contact with potential definitive hosts and contaminated food sources for potential intermediate hosts.

Baylisascaris procyonis larva migrans in two white-headed lemurs (Eulemur albifrons) in Spain and response to treatment derived from a human pediatric protocol.

Baylisascaris procyonis is a well-known ascaridoid nematode that causes larva migrans in humans and many other animal species. The North American raccoon (Procyon lotor) is the definitive host, which has been successfully introduced in the past decades to other geographical regions around the world. Two white-headed lemurs (Eulemuralbifrons) from a Zoological Park in Lugo, Spain, developed severe neurological signs within a brief period after being transferred from exhibit and placed in close contact with three captive raccoons from the same zoo. One lemur was euthanized due to the severity of disease progression and histopathology revealed granulomatous inflammation and ascaridoid larvae in kidneys, lung, spleen and brain. Larvae were identified as B. procyonis larvae by real time PCR. In light of the results, the cage mate with similar neurological signs was put on an albendazole treatment regimen adapted from a human pediatric protocol. The aggressive anthelmintic treatment likely contributed to the arrest of clinical signs and recovery of some motor skills. Importantly, Baylisascaris procyonis infection might occur in wild raccoon populations in Spain.

Echinococcus multilocularis infection of a ring-tailed lemur (Lemur catta) and a nutria (Myocastor coypus) in a French zoo.

Echinococcus multilocularis is a tapeworm responsible in its larval stage for alveolar echinococcosis, a disease which is lethal when left untreated. Multivesiculated parasitic lesions in the liver were diagnosed at necropsy in a captive-born nutria (Myocastor coypus) and in a ring-tailed lemur (Lemur catta) which had been in a French zoo for 16months. Molecular analyses confirmed the diagnosis of E. multilocularis obtained by histological analyses. These were the first cases of infection by E. multilocularis reported in lemurs in Europe, and the first case in nutria in European enclosures. Lemurs are confirmed to be particularly sensitive to E. multilocularis with a massive infection. In both cases, the infection appears to have been contracted in the zoo indirectly via environmental contamination by feces from roaming foxes. Due to the large endemic area for E. multilocularis, the increasing prevalence in foxes in France, and an increase in awareness of the disease, other cases of infection in captive animals will probably be recorded in France in the coming years.

African apes as reservoirs of Plasmodium falciparum and the origin and diversification of the Laverania subgenus.

We investigated two mitochondrial genes (cytb and cox1), one plastid gene (tufA), and one nuclear gene (ldh) in blood samples from 12 chimpanzees and two gorillas from Cameroon and one lemur from Madagascar. One gorilla sample is related to Plasmodium falciparum, thus confirming the recently reported presence in gorillas of this parasite. The second gorilla sample is more similar to the recently defined Plasmodium gaboni than to the P. falciparum-Plasmodium reichenowi clade, but distinct from both. Two chimpanzee samples are P. falciparum. A third sample is P. reichenowi and two others are P. gaboni. The other chimpanzee samples are different from those in the ape clade: two are Plasmodium ovale, and one is Plasmodium malariae. That is, we have found three human Plasmodium parasites in chimpanzees. Four chimpanzee samples were mixed: one species was P. reichenowi; the other species was P. gaboni in three samples and P. ovale in the fourth sample. The lemur sample, provisionally named Plasmodium malagasi, is a sister lineage to the large cluster of primate parasites that does not include P. falciparum or ape parasites, suggesting that the falciparum + ape parasite cluster (Laverania clade) may have evolved from a parasite present in hosts not ancestral to the primates. If malignant malaria were eradicated from human populations, chimpanzees, in addition to gorillas, might serve as a reservoir for P. falciparum.

[Plasmodia of lemurs in Madagascar]. / Plasmodies de lémuriens malgaches.

Lemur macaco macaco from Ambanja region was found polyparasitized by four different species of Plasmodium: --Plasmodium coulangesi recently described by lepers et al. (1989). --P. bucki n. sp.: its main differential characterisitics are the large numvber (32) of merozoites produced in mature schizonts and the stippling, resembling Maurer's dots, in an hypertrophied pinkish erythrocyte. --P. percygarnhami n. sp. (= P. girardi sensu Uilenberg, 1970 pro parte and sensu Garnham et Uilenberg, 1975 pro parte) producing 20 merozoites in mature schizonts and developing inside a deformed corpuscle (holly leaf-shaped or sometimes sea-urchin-shaped) which may also become decolourized when parasitized by older stages. --(?) Plasmodium lemuris: gametocytes are very large (11 microns x 7 micron); the parasitized erythrocyte is much hypertrophied (+/- 10 microns), distored and of a pinkish colour; one schizont only, possibly exo-erythrocytic, was found. The authors hypothesized this parasite to be a Haemoproteid. The analysis of published data led the authors to make the following modifications to the nomenclature previously established: --Plasmodium girardi Buck et al., 1952, sensu Garnham, 1966, sensu Uilenberg, 1970 parte and sensu Garnham and Uilenberg, 1975 pro parte, is refered to as Plasmodium sp., for stages developing in the blood of Lemur fulvus fulvus. The taxon P. percygarnhami is to be employed for stages developing in L. m. macaco and P. girardi Buck et al., 1952 for those developing in Lemur fulvus rufus. --Plasmodium foleyi Buck et al., 1952, sensu Garnham and Uilenberg, 1975 in L. f. fulvus is named Plasmodium uilenbergi n. sp., P. folleyi being a parasite of L.f. rufus. Excluding P. lemuris which probably does not belong to the genus Plasmodium, the morphological analysis led to individualize 7 species, in the three species of Lemurs studied. A phenomenon of "vicariance" thus appears, similar to what is known for the african Rodent Plasmodia, but with a more pronounced speciation. The vicariant species form a pair constituted of: --on the one hand a small species developing in a red blood cell of normal size, P. girardi in L.f. rufus, P. sp. in L.f. fulvus, P. percygarnhami, with also, P. coulangesi, in L. m. macaco; --on the other hand a large species determining an hypertrophy of the erythrocyte, P. foleyi in L.f. rufus, P. uilenbergi in L.f. fulvus and P. bucki in L.m. macaco.