Taenia martis cysticercosis

Deplazes, Peter, Eichenberger, Ramon M. & Grimm, Felix, 2019, Wildlife-transmitted Taenia and Versteria cysticercosis and coenurosis in humans and other primates, International Journal for Parasitology: Parasites and Wildlife 9, pp. 342-358 : 345-348

2.1. Taenia martis cysticercosis

Taenia martis is a large tapeworm of around 20cm in length that develops in the small intestine of wild carnivores, mainly Mustelidae . In North America, T. martis americana has been described in Martes americanum (Hoberg et al., 1990) . In Europe, it was described in the stone marten ( Martes foina ) and in the pine marten ( M. martes ). However, other mustelids and rarely canids and felids might also act as definitive hosts ( Table 1). Taenia martis is transmitted in a wild-animal cycle between mustelid carnivores and their pray, including rodents and other small mammals as intermediate hosts. In the intermediate hosts the larval form (cysticercus) reaches a size of 6–32mm (more details see diagnostic section). It mainly develops in the pleural and peritoneal cavity as a pseudo segmented larva, not surrounded by a fibrous capsule, and without asexual multiplication ( Schuster and Benitz, 1992).

In Europe, T. martis has been observed in martens in Italy ( Millan et al., 2001), Belgium ( Mathy et al., 2009) Poland ( Kornaś et al., 2013) and Belarus where it has also been detected in the European polecats ( Shimalov, 2010). In Southwestern Germany, T. martis was found in 1 (0.03%) of 3573 red foxes, in 2 (2.2%) of 84 badgers ( Meles meles ) and in 17 (37%) of 47 stone martens ( Loos-Frank and Zeyhle, 1982). In southwestern Yakutia (Sibiria) between 1981 and 1987, T. martis was found in 28% of 272 and 30% of 1548 Martes zibellina , respectively (Sedalischev and Odnokurtsev, 2011; Odnokurtsev and Sedalischev, 2011).

Taenia martis cysticercosis in rodents seems to occur all over Europe but focally in variable prevalence. As an example in Eastern Switzerland, T. martis larval stages (cysticerci) were detected in 43 (10.5%) of 411 Apodemus flavicollis , in 100 (7.8%) of 1276 A. sylvaticus and in 294 (24.3%) of 1211 Myodes (syn. Clethrionomys ) glareolus , but not in 894 Arvicola terrestris , 347 Microtus arvalis and 250 M. agrestis of the same area ( Schaerer, 1987). In contrast, in Western Switzerland (Geneva) T. martis was found in 2 of 99 A. flavicollis , but not in 466 A. terrestris , 58 M. glareolus and 35 M. arvalis ( Reperant et al., 2009). Comparable low prevalence of T. martis were found in Berlin, Germany (1.4% of 59 M. glareolus, 78 Apodemus agrarius and 82 A. flavicollis ) ( Krücken et al., 2017), and in Western France in nutria ( Myocastor coypus ) ( Umhang et al., 2013). In Germany, muskrats ( Ondatra zibethicus ) were highly infected with T. martis cysticerci ( Loos-Frank and Zeyhle, 1981), similar to the Limburg region in the Netherlands (18.6% of 526 muskrats), but in contrast to animals from Groningen (n=1200) with a prevalence of merely 0.7% ( Borgsteede et al., 2003). From Ireland, Loxton et al. (2017) reported a prevalence of T. martis of 0.77% (CI: 0·16–2·24) in wood mice ( A. sylvaticus ). Reports from northern Spain document the occurrence of T. martis in 0.7–1.0% of 376 M. glareolus ( Ribas et al., 2009). In Serbia 4.1% of 588 M. glareolus were infected with T. martis ( Bjelić-Čabrilo et al., 2011) . In Belarus, the redbacked vole, the striped field mouse and the yellow-necked mouse are hosts of this helminth ( Shimalov, 2010), and recently it was documented there as a parasite of red squirrels (Sciurus vulgaris Linnaeus, 1758) ( Shimalov, 2016).

To our knowledge, four cases of human T. martis cysticercosis have been reported in immunocompetent women ( Table 3). Interestingly, three of these patients originated from Alsace ( France) and Western Germany, while the remaining fourth case was described in northern Germany. In these cases, cysticercosis manifested itself as a solitary lesion in the brain, in the peritoneum and in two cases in the eye. Furthermore, two cases in non-human primates, one originating from

Alsace, the other from a zoo in Rome ( Italy), presented as abdominal T. martis -cysticercosis ( Table 4). Finally, in a 14-year-old Frenchman and a 15-year-old Austrian woman, ocular cysticercoses caused by juvenile taeniid larvae could not be morphologically specified ( Table 3). Similarly, a cysticercosis with fully developed cysticerci isolated from the abdomen of a lemur from a zoo in the USA in 1989 was diagnosed as Taenia sp. cysticercosis ( Table 4).

Routes of human infections can only be speculated about. Two patients were recreational gardeners and could have been exposed to marten faeces during such activities. Extensive recreational hiking in

Taenia sp. , case no., Primate species, patient, origin, and case history Pathological findings Etiological diagnosis: morphology and DNA citation analysis (PCR, sequencing) a

Taenia crassiceps Hamadryas baboon ( Papio hamadryas ) “no Necropsy. Larval stages subcutaneously and in Morphology. Diagnosis based on number

Case 1, individual data available”, lived in a group in the the smooth muscles, penetrating to the (n=30–35) and size (large 182–200, small Baer and Zoo Basel, Switzerland, together with a couple of retroperitoneal cavity, with parasite infiltration 138 <150μm) of rostellar hooks and Scheidegger (1946) foxes.The animal was necropsied after a history of into the spinal cord. budding of the cysticerci.

tetraplegia. DNA analysis. Nd.

T. crassiceps Adult female black lemur ( Eulemur macaco macaco ) Necropsy. Fluctuant swelling measuring 10cm Morphology. Cysticerci with calcareous

Case 2, with a clinical history of lethargy, anorexia, and by 6cm on the left back. A well-defined cystic corpuscles, a scolex with a rostellum with

Dyer and Greve depression of a week's duration was submitted for structure contained hundreds of ellipsoidal to hooks, spinous tegument, and exogenous (1998) necropsy. The animal was housed outdoors in a spherical cysts of 1–4mm in diameter. budding.

group. Infiltration of both the peritoneal and pleural DNA analysis. Nd.

cavities by large numbers of cysticerci were found replacing approximately 90% of the left lung.

T. crassiceps 6-year-old female red ruffed lemur ( Varecia Radiographs of the cervical region showed the Morphology. A wet-prep of the nodules

Case 3, variegata rubra ) with 2 days history of lethargy and mass containing discrete areas of revealed cestode larvae. Histopathology. A Young et al. (2000) anorexia was presented with a large, fluctuant mineralization. Surgical exploration “revealed a single mass was described as granulomatous subcutaneous swelling extending from the dorsal multiloculated mass with each individual cyst- cellulitis with intralesional larval cestodes.

aspect of the skull to the ventral cervical region. like structure containing hundreds of bead-like DNA analysis. Nd.

nodules (<1mm)”.

T. crassiceps 5-year-old male, ring-tailed lemur (Lemur catta ) in US image of the swelling suggested a septated Morphology. Based on the scolex and hooks Case 4, the Madrid Zoo-Aquarium, Spain, presented a large subcutaneous mass. Exploratory surgery and budding was observed.

Luzón et al. (2010) swelling in its abdomen (15cm in length× 10cm revealed an irregular fibrous cystic structure, DNA analysis. cox1 [P1] and nd1 [P3]:

in width× 4cm in height) and was anesthetized for containing numerous small transparent vesicles Identities 99–100% with corresponding a complete medical evaluation. (ca. 3mm in diameter) and after the peritoneal published T. crassiceps sequences.

cavity was opened more vesicles were extirpated.

T. crassiceps 15-year-old female ring-tailed lemur ( L. catta ) from Necropsy. “large multicystic structure, Morphology. Cysticerci with single inverted Case 5, Sarajevo Zoo, Bosnia and Herzegovinawas was subdivided with fibrous septa and filled with scolex, a rostelum with two rows of hooks and Alić et al. (2017) presented after sudden death numerous translucent, oval to ellipsoid bladder- exogenous buds.

like cysts, almost completely replacing right DNA analysis. cox1 [P2]: Identity 880/

lung lobe “. 880bp, 100% with T. crassiceps (GenBank

AF216699, AB033411).

T. crassiceps 28-year-old female, captive-born Nilgiri langur Necropsy. Skeletal muscle of the left thigh had Morphology. Based on hook morphology.

Case 6, ( Semnopithecus johnii ) from a German zoo, with a been replaced by a multilocular cystic mass DNA analysis. cox1 [P1]: Identities 98–100% Bleyer et al. (2018) right ankle joint age-related myxosarcoma containing numerous sand-grain–sized whitish (450 bp) with T. crassiceps sequences.

developed an edematous swelling of the left thigh structures; similar cysts were also present in the and also suffered from lethargy and anorexia. lung and the myocardium.

Animal was euthanized because of poor general condition.

Taenia serialis Gelada baboon ( Theropithecus gelada ) from the Necropsy. Large subcutaneous tumor (1.5kg). Morphology based on larval hooks and of Case 1, National Zoological Park at Washington, D. C, with The majority of the mature cysts contained adult worms from experimentally infected Schwartz (1927) a large subcutaneous tumor in the right thoracic several hundred scoleces. dogs.

region. DNA analysis. Nd.

T. serialis Juvenile (<2 years) spotted-nose monkey Necropsy.Many discolored bodies (1–2cm) Morphology. Microscopical examination

Case 2, ( Cercopithecus nictitans ) imported from the West attached to mesentery. Scalp with bone erosion corresponds to Coenurus serialis .

Sandground (1937) African Coast to the USA as a pet animal. Slight and protrusion of a mass of translucent, white DNA analysis. Nd.

torticollis for 3–4 weeks, soft swelling at the back of cysts.

the head. Died.

T. serialis 4-year-old gelada baboon ( T. gelada ), borne in Necropsy. Multiple subcutaneous nodules in Morphology. Diagnosis of cysts (no

Case 3, captivity in Germany and imported to USA upper and lower extremities (1–12cm), and a microscopic details provided).

Elek and Finkelstein (zoological park). Spastic paralysis in right lower large intra-abdominal cystic mass infiltrating DNA analysis. Nd.

(1939) extremity before death. underlying muscles.

T. serialis Male gelada baboon ( T. gelada ), transported Necropsy. Subcutaneous nodular enlargement Morphology. Diagnosis of cysts (no

Case 4, between two zoological parks in the USA. Nodular (11–25cm) with small ulcerations. microscopic details provided). Infection of 2 Clark (1969) enlargement on right thigh. Euthanized because dogs was not successful.

surgery was not successful. DNA analysis. Nd.

T. serialis 13-year-old male, wild Ethiopian gelada baboon (T. Small to large swellings in various parts of the Morphology. Not reported.

Case 5, gelada ) from a national park. Tissue was extracted animal's body. DNA analysis. Its2 [P9] and 12S [P5]: 99% Schneider-Crease from a protuberant coenurus on the left ventral and 99% identity with T. serialis sequences.

et al. (2013) forelimb.

T. multiceps 6-year-old female gelada baboon ( T. gelada ) from a Necropsy. Multilocular easily ruptured cystic Morphology. Size, number, and shape of (probably zoological park in the USA. Animal, which was masses in the left masseter and temporal muscle hooklets provided by the author, but misdiagnosed) imported from Ethiopia with 2 years, presented region. Further subcutaneous cysts in the inconclusive according to Table 5.

Leith and Satterfield multiple subcutaenous cysts. scapular region extending into the abdomen. DNA analysis. Nd.

(1974)

T. brauni b Rhesus monkey ( Macaca mulatta ), kept in France Necropsy. Abdominal tumor at left perineum Morphology. Microscopical measurements Railliet and but unknown origin, infected with Leishmania (2.7–5cm). performed. b

Marullaz (1919) tropica, died in experiment. DNA analysis. Nd.

Monkey ( Cercopithecus mitis doggetti ), Rwanda

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Table 4 (continued)

the Alps was reported from another patient but without obvious contact to wild animals. All four patients could successfully be treated by surgery and anthelminthics.

Interestingly, all T. martis -cysticercosis patients described so far originated from Europe, and no data are available on the zoonotic potential of T. martis americana . Furthemore, all four human T. martis cases were documented in 36, 43, 44 and 70 years old women, though the number of cases is too small to speculate on a gender association. However, the host's endocrine system can have an impact on the susceptibility to cestode infections. For example, castration of male and pregnancy in female pigs significantly increased the prevalence of naturally acquired T. solium cysticercosis ( Morales et al., 2002), female mice are more susceptible to experimental infections with T. crassiceps than males ( Morales-Montor et al., 2002), and female rabbits are more frequently infected with T. pisiformis metacestodes than males ( Domínguez-Roldan et al., 2018).