Taenia multiceps coenurosis

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 : 351

3.2.2. Taenia multiceps coenurosis

Taenia multiceps (formerly Multiceps multiceps ) is a large tapeworm with variable size between 20 and 120cm. Taenia multiceps coenurosis (sometimes called gid, staggers, or sturdy) has been documented in scattered foci all over the world, with the exception of Australia and New Zealand ( Scala and Varcasia, 2006). In North America, however, the last case of T. multiceps gid has been reported in the thirties and the disease is considered absent, despite one supposed human case in 1982 ( Becklund, 1970; Ing et al., 1998; Schellhas and Norris, 1985).

The parasite life cycle is predominantly maintained by domestic and stray dogs, when they have access to residuals from improper discarded slaughtered meat, or roaming of stray dogs around small ruminant farms and early access to animals that died in the field ( Abera et al., 2016; Vasileiou et al., 2015). Global transport of domestic dogs (travel and trading) represents yet another risk for the dissemination of taeniid eggs. Correspondingly, in Switzerland where only rare and sporadic cases are noticed, an outbreak of coenurosis in a dairy sheep flock has been reported, with approx. 10% of 140 sheep presenting clinical signs. The source of infection was a single livestock guardian dog imported from Italy ( Schweizer et al., 2006).

The importance of wild carnivores for the distribution of taeniid eggs is valid where wild canids (e.g. wolves and foxes) have access to animals that have died in the field infected with T. multiceps . The role of wild carnivores was neglected as it was assumed that they have no access to sheep brains protected by the thick skull. However, firstly, the presence of cysts is associated with thinner skull bones, thus allowing access, even for foxes ( Scala and Varcasia, 2006). Secondly, infection trials have demonstrated that foxes can develop gravid proglottis and infective eggs ( Varcasia et al., 2015b). Correspondingly, in various regions where T. multiceps coenurosis is endemic in sheep, tapeworms have been reported from fox species, with 1–28.2% positive results from necropsied foxes in Russia (summarised in Varcasia et al., 2015b), 0–5% in Germany ( Ballek et al., 1992; Loos-Frank and Zeyhle, 1982; Welzel et al., 1995), 2% in Peru ( Moro et al., 1998), 3.8% in Jordan ( El-Shehabi et al., 1999), 4.8–8.2% in Iran ( Dalimi et al., 2006; Nabavi et al., 2014), and 6% in Tibetan sand foxes in China ( Li et al., 2013). An extensive survey on fox hounds and foxes in Wales revealed 0.46%–1.7% dogs infected with T. multiceps but none of the foxes ( Jones and Walters, 1992 a, 1992b). However, the foxes had other Taenia species, including T. serialis which is responsible for coenurosis in lagomorphs in the UK (see below). In addition, earlier publications demonstrate the presence of T. multiceps in foxes in Bulgaria, Czech Republic, Italy, Poland and Switzerland (summarised in Loos-Frank and Zeyhle, 1982).

The wolf is a known definitive host for T. multiceps and T. serialis ( Craig and Craig, 2005; Otranto et al., 2015b). Data are available for European grey wolf populations with prevalences of 0.5% in Croatia ( Hermosilla et al., 2017), 3.9% in Serbia ( Cirovic et al., 2015a), 0–9% in Italy ( Gori et al., 2015; Guberti et al., 1993; Paoletti et al., 2017), 27% in Estonia ( Moks et al., 2006), 28–29.8% in Spain ( Segovia et al., 2001, 2003), and up to 47.1% in Latvia ( Bagrade et al., 2009). Nabavi et al. (2014) found 1 of 4 wolves from Iran positive for T. multiceps . Interestingly, golden jackals ( C. aureus ) from Italy as well as from the western part of Iran were negative for T. multiceps and T. serialis ( Dalimi et al., 2006; Nabavi et al., 2014; Paoletti et al., 2017). In Serbia, however, T. multiceps was found in 1.6% of golden jackals, another wild carnivore of eastern Europe, the Middle East and Asia ( Cirovic et al., 2015b). These tapeworm species were absent in 80 brown bears in a T. multiceps / T. serialis endemic region in central Italy ( Paoletti et al., 2017). Henke et al. (2002) described T. multiceps in coyotes in Texas but this report needs to be considered with care as it could be a morphological miss-diagnosis of T. serials , and generally T. multiceps is assumed to be abset in North America.

Metacestode infections (coenurosis) have also been reported from dead-end hosts (including dogs, horses, humans and other primates). Taenia multiceps coenurosis in humans and other primates represents a serious clinical condition. Supplemental Table 1 summarizes 45 cases of human T. multiceps- coenurosis, which were from Africa (n=21), Europe (n=17), Asia (n=2), South America (n=1), USA (n=3) and the Middle East ( Israel; n=1). Where specified, the age of the patients was between 1 and 55 years (median: 33; SD: 17.0), showing that all age groups are potentially affected. Similar to infections in ruminants, the predominant infected tissue was the brain (n=35/44), followed by intra-/periocular infections (n=8/44) and rarely infections in the spinal cord (n=1/44). Correspondingly, the infection was often fatal (42%) or ended with the loss of vision after eye removal (15%). Symptoms like partial paresis or paraplegia remained (12%), and only one third of the patients recovered partially or completely after surgery. However, in spite of the severity of the outcome of an infection in humans, coenurosis represents a rather minor risk for public health, given the relatively high infection pressure demonstrated by the wide occurrence and high prevalence of T. multiceps in canids but only 5 published cases in the past 25 years. Furthermore, there are no indications of immunodeficiency in these cases. Similarly, T. multiceps is rarely reported in other primates.