Taenia crassiceps 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 : 349-350

3.1. Taenia crassiceps cysticercosis

Taenia crassiceps is a relatively large but harmless tapeworm, 10–22cm in length, inhabiting the intestines of carnivore definitive hosts, and it is widly distributed in the northern hemisphere ( Table 1). In rodents, which are the natural intermediate hosts for the parasite, the larval (metacestode) form of T. crassiceps has a particular asexual reproduction by budding both exogenously and endogenously ( Baer and Scheidegger, 1946, Freeman, 1962; Slais, 1973). Exogenous budding at the abscolex pole can produce 1–6 daughter cysticerci, which can bud off or remain attached and form a scolex of their own. This continuous and uncontrolled proliferation leads to massive infections, most frequently involving the subcutis, and both pleural and peritoneal cavities, causing death of the intermediate host within several months, or serious pathological implications in a large variety of dead-end hosts, including humans and other primates. Sporadic cases of cysticercosis caused by T. crassiceps have been documented in humans ( Table 2), non-human primates (Tabel 4), but also rarely in e.g. domestic dogs ( Ballweber, 2009; Beugnet et al., 2009; Chermette et al., 1993; Hoberg et al., 1999), a cat ( Wunschmann et al., 2003), red foxes ( Konjević et al., 2016; Whipp et al., 2017) and a chinchilla (Chincilla lanigera) ( Basso et al., 2014).

Natural intestinal infections with T. crassiceps have been described in the northern hemisphere mainly in the red fox ( V. vulpes ), but also in several other canids. A study in New Brunswick and Nova Scotia in eastern Canada in red foxes reported prevalences of 50% for T. crassiceps ( Smith, 1978) . T. crassiceps was also reported from Greenland ( Andreassen et al., 2017), from Svalbard island ( Stien et al., 2010), and from China, with 2 of 27 red foxes, and 1 of 9 Tibetan sand foxes found infected ( Li et al., 2013).

In European red foxes T. crassiceps is widely distributed with prevalence varying between 4.3 and 29%, and 7.6% in foxes living in the city of Zurich, Switzerland ( Hofer et al., 2000). Similar prevalence ranges have been described for Germany (17.7–28.5%, Ballek et al., 1992; Loos-Frank and Zeyhle, 1982; Pfeiffer et al., 1997; Welzel et al., 1995), France (15.9–29%, Pétavy and Deblock, 1980; Pétavy et al., 1990), Spain (4.3–23%, Alvarez et al., 1995; Segovia et al., 2004), and Lithuania (26.4%, Bruzinskaite-Schmidhalter et al., 2012). In Russia, 19% of 68 hunted red foxes were infected with T. crassiceps in central Yakutia ( Sedalischev and Odnokurtsev, 2013), and 49% of 247 red foxes and 7% of 43 corsac foxes ( V. corsac ) of Omsk Oblast (Siberia) between 2000 and 2004 ( Bukova, 2006).

Taenia crassiceps was also detected in wolves in Canada, Europe and Russia ( Abuladze, 1970; Craig and Craig, 2005). In Latvia 9% of 34 ( Bagrade et al., 2009), and in North-West Caucasia 2.8% of 36 wolves were infected with T. crassiceps ( Itin et al., 2018) . Freeman (1961) detected T. crassiceps in 1.7% of 58 Canadian wolves and in one of 6 coyote-dog hybrids, but not in 68 coyotes.

Of 17 Hungarian golden jackals ( Canis aureus L., 1758), T. crassiceps has been found in 40% ( Takács et al., 2014) and infections were recorded in 0.6% of 179 wolves in northern Italy ( Gori et al., 2015). The raccoon dog ( Nyctereutes procyonoides ) seems to be another suitable host of T. crassiceps : it was identified in 6 of 72 animals from the Republic of Belarus ( Subbotin, 2009), and it was found in 3.5% of 85 raccoon dogs in Lithuania ( Bruzinskaite-Schmidhalter et al., 2012).

However, not only canids seem to be susceptible to T. crassiceps intestinal infections. Raccoons ( Procyon lotor ) were infected with T. crassiceps as reported from the North-Western Caucasus with a prevalence of 24% in 42 animals ( Itin et al., 2018). Schuster et al. (1993) identified T. crassiceps tapeworms in 2 of 25 wild cats ( Felis silvestris ) and Loos-Frank and Zeyhle (1982) found infections in 6% of 47 stone martens ( Martes foina ) in Germany.

Finally, in several human patients with T. crassiceps cysticercosis, close contacts to domestic dogs were assumed as source of infection (cases 1, 4, 5, 8, 10; Table 2). However, the epidemiological importance of domestic carnivores is probably overestimated. Umhang et al. (2014) reported 5 of 817 (0.6%) dog faecal samples from eastern France to be positive for T. crassiceps eggs. Dyachenko et al. (2008) detected T. crassiceps eggs in 7 of 17,894 (0.04%) dog samples in Germany and other European countries, but in none of 9064 cat faeces. However, in an older study in southwest Germany intestinal infections with T. crassiceps were also observed in 1% of 387 stray cats supplied for rabies examination, some had been shot by private hunters and some were road kills ( Loos-Frank and Zeyhle, 1982).

As intermediate hosts in northern America, the muskrat ( Ondatra zibethicus ), the common vole ( Microtus arvalis ), the eastern chipmunk ( Tamias striatus ), the deer mouse ( Peromyscus maniculatus ), the meadow vole ( Microtus pennsylvanicus ), but also the woodchuck ( Marmota monax ), and lemmings ( Dicrostonyx groenlandicus richardsonii , Lemmus trimucronatus trimucronatus ) were identified ( Leiby and Whittaker, 1966; Albert et al., 1972). In Europe T. crassiceps cysticercosis seems to occur focally in variable prevalence in rodents. In Switzerland, T. crassiceps cysticerci were detected in 2 (0.22%) of 894 Arvicola terrestris , in 3 of 347 (0.86%) Microtus arvalis , and in 1 (0.4%) of 250 M. agrestis, but not in 411 Apodemus flavicollis , 1276 A. sylvaticus and 1211 Myodes (Syn. Clethrionomy) glareolus of the same area in eastern Switzerland ( Schaerer, 1987). These very low prevalence of T. crassiceps , as well as very low prevalence of E. multilocularis (0.11%) in A. terrestris , and the absence in the other species mentioned above, were probably associated with the significantly reduced fox population during this time, which was attributed to the rabies epidemic and the corresponding control measurements. Later studies reported higher T. crassiceps prevalence, e.g., in 2.0% of 889 A. terrestris , whereas none were detected in neither 83 M. glareolus nor 154 Apodemus sp. ( Stieger et al., 2002), while another study found T. crassiceps in 1.9% of 856 A. terrestris ( Burlet et al., 2011) in the Zurich Area ( Switzerland). In the Geneva area ( Switzerland) Reperant et al. (2009) detected T. crassiceps cysticerci in 2.6% of 466 A. terrestris , in 2.9% of 35 M. arvalis, and in 1.0% of 99 A. flavicollis , but not in 58 M. glareolus. Interestingly, no T. crassiceps or T. taeniaeformis were identified in a study in Berlin ( Germany), including 77 A. flavicollis , 25 A. sylvaticus , 72 A. agrarius , 56 M. glareolus, and 10 Microtus sp. ( Krücken et al., 2017). Finaly, in Japan T. crassiceps was found in three of 46 M. montebelli but not in 187 Apodemus speciosus ( Ihama et al., 2000) .

Interestingly, no reports on the occurrence of T. crassiceps were found from Scandinavia, Ireland and the UK. No T. crassiceps infections were detected in 197 foxes from Wales ( Jones and Walters, 1992a), in 843 foxes from Southern England ( Richards et al., 1995), and in 366 foxes from Northern Ireland ( Ross and Fairley, 1969). Furthermore, in this paper the intestinal helminths in foxes in the UK were reviewed and T. crassiceps was not mentioned in several older studies. Further, no T. crassiceps findings are mentioned in rodent investigations in Zealand, Denmark ( Al-Sabi et al., 2015; Tenora et al., 1991), in 1702 rodents investigated in Sweden ( Miller et al., 2016), nor in high numbers of rodents investigated in Finland ( Tenora et al., 1983; Soveri et al., 2000), and Ireland ( Loxton et al., 2017).

Because of the high T. crassiceps prevalence in red foxes and their high population densities, the fox seems to be responsible for the perpetuation of the parasite cycle, as well as for the contamination of the environment with eggs in Central Europe. A similar situation can be observed with E. multilocularis ( Hegglin and Deplazes, 2013) . However, only a few studies have documented environmental contamination with T. crassiceps eggs. For example, Hauser et al. (2015) identified T. crassiceps eggs through DNA analyses in 5 (8.6%) of 58 fox faecal samples,

and in one (0.2%) of 402 dog samples collected during the course of one year in 14 different grassland areas in the canton of Zurich, Switzerland. Furthermore, T. crassiceps eggs have been identified in the washing water of one of 141 samples of food, which consisted each of around 40 heads of lettuce, as well as various vegetables and fruits ( Federer et al., 2016).

A number of well documented cases of T. crassiceps cysticercoses have been published in humans and other primates ( Tables 2 and 4). Most of the cases, which have all been published in the last 30 years, originated from Central Europe ( Germany, Switzerland, and France). Most cases of humans involving subcutis and muscles have been associated with underlying immunosuppression (cases 2, 3, 5–8; Table 2), except case 9, where a subcutaneous infection was associated with a haematoma localized on the right temple in an immunocompetent Swiss patient, and case 12 where a subcutaneous infection on the shoulder of a patient from USA was documented ( Table 2). In contrast, an intercerebellar (case 10) or intraocular infections (cases 1, 4, and 11; Table 2) were not associated with an impaired immune system.

Surprisingly, in all cases, the infection started uni-focally and progressed by infiltration of the surrounding tissues, especially in the nonocular/neural cases. Due to the systemic spread of the activated oncospheres in the blood circulation after oral egg uptake we would expect simultaneous multifocal infections as described for T. solium (especially in severely immunocompromised patients) and for T. serialis , where in some cases multiple lesions were observed in individuals without any indication of immuno-suppression. Interestingly, among the 7 cases of subcutaneous T. crassiceps cysticercosis ( Table 2), 5 had a history of precedent injuries associated with the later development of cysticercosis. In cases 2, 3, 6, 7 a haematoma after a fall was reported at the site of subsequent cysticercosis development. In case 8, the patient remembered, that 5 months before the swelling on the same arm started, an injury to her right wrist occurred during her work as a zoo-employee.

Generally, humans acquire taeniid infection by oral ingestion of infective eggs. The most probable route of transmission after contact with taeniid eggs in the contaminated environment is the hand-tomouth route. Hypothetically, transmission has also been linked to water or food-borne sources (vegetables/fruit/berries), but any source attribution is uncertain ( Alvarez-Rojas et al., 2018). Taeniid eggs can be dispersed from carnivore faeces with water or by adhering to objects (e.g. shoes and tyres). For example E. multilocularis eggs have been found on the hair coat of foxes ( Nagy et al., 2011), suggesting a variety of potential infection routes to humans.

There is experimental evidence that taeniid eggs can hatch and develop further without the gastric passage. In sheep it was demonstrated that intra-tracheal E. granulosus egg inoculation was followed by cystic echinococcosis development in the lungs ( Thompson, 1995). Furthermore, embryophore-free (based on sodium hypochlorite treatment) but not enzymatically activated E. multilocularis oncospheres caused local alveolar echinococcosis after subcutaneous injection in a mouse model designed for the documentation of egg viability ( Federer et al., 2015). The same method using 1000 T. crassiceps eggs resulted in subcuataneous cysticercosis (confirmed by PCR/sequencing as described in Trachsel et al., 2007) in 2 of 3 inoculated BALB/c mice (Joekel D. and Deplazes P., unpublished data). Therefore, taeniid eggs accidently contaminating cutaneous injuries might locally hatch and further develop to larval stages. A human case of subcutaneous alveolar echinococcosis ( Tschudi and Ammann, 1988) associated with a cutaneous injury, and a subcutaneous cystic echinococcosis in the popliteal fossa at the site of a previous wasp sting ( Battyany et al., 2010), have been documented.