28-year-old, female, Nilgiri langur, (Trachypithecus johnii).An adult female captive born Nilgiri langur (Trachypithecus johnii) from a zoological garden in Central Europe developed an edematous swelling of the left thigh, which persisted for several months and was associated with periods of a decreased general condition, depression, and anorexia. Sonographic examination of the thorax and abdomen revealed cardiomegaly as well as poor demarcation and cloudy appearance of the liver. The animal was finally euthanized due to a poor general condition, anorexia, and therapeutic resistance.

Gross Description:  

At necropsy, the animal was cachectic. The skeletal muscle of the left thigh was severely atrophic and replaced by fluctuant multilocular cysts containing numerous sand grain sized whitish structures.  The left caudal lung lobe revealed a focal circumscribed area of atelectasis.

Histopathologic Description:

Within the skeletal muscle of the left thigh are multifocal extensive areas of fibrous connective tissue bearing multiple cystic structures with numerous larval cestodes (cysticerci). Cysts are surrounded by thick fibrous capsules that are multifocally infiltrated by plasma cells, lymphocytes, macrophages, and eosinophils. The inflammatory cells extend into the adjacent fibrous granulation tissue between muscle fibers that contains few multinucleated giant cells. Cysticerci are characterized by a 4 µm thick, eosinophilic tegument, a fibrillar, eosinophilic parenchyma, numerous 5 µm diameter, basophilic, calcareous corpuscles, and an invaginated scolex with muscular suckers and hooks.

Morphologic Diagnosis:  

Skeletal muscle: Myositis, chronic, gran-ulomatous and eosinophilic, multifocal, severe, with intralesional cysticerci, Nilgiri langur (Trachypithecus johnii), non-human primate.

Lab Results:  

PCR analysis of muscular metacestode tissue identified Cysticercus longicollis, the larval stage of Taenia crassiceps, as the etiologic agent.


Cysticercus longicollis, langur

Contributor Comment:  

Non-human primates might act as aberrant hosts for a number of cestode species after oral infection and larval development in extra-intestinal locations.2  Taenia crassiceps is a cestode parasite of the Northern hemisphere, whose life cycle includes canids as definitive hosts, most commonly the red fox (Vulpes vulpes) in Europe and the Artic fox (Alopex lagopus) as well as the red fox in North America.6 Natural infection by T. crassiceps has also been reported in wolves (Canis lupus)5 and coyotes (Canis latrans)13 in North America as well as in wild cats (Felis silvestris)12 and domestic dogs in Germany.3 Several rodent species and rabbits serve as intermediate hosts for the metacestode larval stage of the parasite, Cysticerus (C.) longicollis. However, the common vole (Microtus arvalis) is the predominant intermediate host in Europe.1 Sporadic cases of clinical cysticercosis caused by T. crassiceps have been reported in humans and domestic animals such as dogs and cats, many of them in immuno-compromised individuals.8,9,16 Infections by T. crassiceps may be particularly serious due to their proliferative nature. In contrast to cysticercosis associated with other Taenia species, T. crassiceps is able to proliferate by exogenous and endogenous budding. Exogenous budding may produce 1-6 daughter cysticerci at the abscolex pole of the maternal cyst. Daughter cysticerci may bud off or remain attached by a stalk, form a scolex of their own, and bud again. Endogenous budding occurs less commonly and is seen in larger, older cysticerci. Such reproductive capability may result in extensive infections, most frequently involving the subcutis and pleural and peritoneal cavities. In humans, there are occasional reports about intraocular mani-festations of cysticercosis.4
In non-human primates, there are documented cases of T. crassiceps cysticercosis in a black lemur (Eulemur macaco macaco)4 and in a ring-tailed lemur (Lemur catta)10, both of them being prosimian species. T. crassiceps cysti-cercosis in an Old World monkey species like the Nilgiri langur has not been reported before. Interestingly, in the langur, metacestode tissue was not limited to the skeletal muscle, but could also be observed in the left caudal lung lobe, reflecting the proliferative and invasive nature of this parasite.
Other Taenia species causing cysticercosis in non-human primates include Taenia solium, Taenia crocutae, Taenia hydatigena, and Taenia martis.2,14 However, infections with the larval cestodes mainly occur in Old World monkeys and apes, while reports of taeniid cysticercosis in New World monkeys and prosimians are sparse.
Studies on the immune response elicited by T. crassiceps and its antigens in human and mice cells suggest a strong capacity of this parasite to induce a chronic Th2-type response that is primarily characterized by high levels of Th2 cytokines, a low proliferative response in lymphocytic cells, an immature and LPS-tolerogenic profile in dendritic cells, recruitment of myeloid-derived suppressor cells, and by activated macrophages.11

JPC Diagnosis:  

Skeletal muscle: Cysticerci, multiple, with mild chronic granulo-matous inflammation, Nilgiri langur (Trachypithecus johnii).

Conference Comment:  

The contributor provides a striking example of multiple intramuscular cysticerci containing cross sections of taeniid metacestodes, the larval form of cestode tapeworms. The class Cestoda has two orders of veterinary importance. The first is Pseudophyllidea, comprised of Diphyllobothrium sp. and Spirometra sp.15 These parasites grow into extremely large adults, up to 15 meters in humans, lack suckers, and require two intermediate hosts, typically an aquatic copepod and fish. In contrast, the order Cyclophyllidae, which contains Taeniidae, Mesocestoididae, Dipylidiidae, Ano-plocephalidae, and Hymenolepididae, require only one intermediate host, usually a land mammal or arthropod.15 Adult cestodes are normally present in the intestine, hepatic ducts, and/or pancreas of the final definitive host while the larval forms are present within the tissue or body cavities of intermediate hosts. Adult cestodes are broken into segments, called proglottids, which contain both female and male reproductive organs. Cyclophyllidae have four anterior suckers present in both larval and adult cestodes and birefringent armed hooks, depending on the species. The four anterior suckers may not all be visible histologically due to varying planes of section.7,15
While adult tapeworms are usually of minor significance in their carnivorous definitive hosts, the larval form can migrate into various tissue and cause significant pathology in intermediate or paratenic hosts. Conference participants discussed the four different forms of larval cestodes in tissue section. These include cysticercus, present in this case, strobilocercus, coenurus, and the hydatid cyst.7,15 The cysticercus is thin walled, fluid filled, and contains a single larva with one inverted scolex and four suckers. The strobilocercus is later in development and contains an evaginated and elongated scolex and develops multiple segments, similar to the adult cestode. Coenurus is similar to cysticercus but contains more than one scolex, all of which can develop into an adult in the definitive host. Hydatid cysts, typical of the genus Echinococcus sp., have a bladder with large numbers of small protoscolicies grouped into clusters called brood capsules.7,15
The inflammatory response in this case is mild and composed of a mixed population of histiocytes, multinucleated giant cell macrophages, lymphocytes, and plasma cells with mild atrophy of the adjacent skeletal muscle bundles. The glycoprotein-rich wall of the cysticerci provokes little to no host reaction when intact; however, rupture of the cysticerci results in a severe granulomatous inflammation, fibrosis, and mineralization.15 Additionally, Cysticercus longicollis, the larval form of Taenia crassiceps present in this case, undergoes both endogenous and exogenous budding of the cysticerci leading to severe and disseminated infection.4


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6. Freeman RS. Studies on the biology of Taenia crassiceps (Zeder, 1800) Rudolphi, 1810 (Cestoda). Can J Zool. 1962;40:969-990.
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8. Hoberg EP, Ebinger W, Render JA. Fatal cysticercosis by Taenia crassiceps (Cyclophyllidea: Taeniidae) in a presumed immunocompromised canine host. J Parasitol. 1999;85:1174-1178.
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11. Peón AN, Espinoza-Jiménez A, Terrazas LI. Immunoregulation by Taenia crassiceps and its antigens. Biomed Res Internat. 2013. doi:  10.1155/2013/498583.
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15. Uzal FA, Plattner BL, Hostetter JM. Alimentary system. In: Maxie MG ed. In: Jubb Kennedy and Palmer's Pathology of Domestic Animals. Vol 2. 6th ed. Philadelphia, PA: Elsevier Saunders; 2016:221-225.
16. Wüschmann A, Garlie V, Averbeck G, et al. Cerebral cysticercosis by Taenia crassiceps in a domestic cat. J Vet Diagn Invest. 2003;15:484-488.

Click the slide to view.

3-1. Skeletal muscle, langur.

3-2. Skeletal muscle, langur.

3-3. Skeletal muscle, langur.

3-4. Skeletal muscle, langur.

3-5. Skeletal muscle, langur.

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