Coenurus serialis, Gervais, 1847

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 : 352

3.2.3. Taenis serialis coenurosis

The adult T. serialis tapeworm has a size of 20–72cm and is morphologically very similar to T. multiceps but can be differentiated by hook number, size, and shape (Table 5). The life cycle of T. serialis includs canids as final hosts and hares and rabbits (rarely rodents) as intermediate host ( Table 1), with Coenurus serialis in subcutaneous and muscle tissues, and occasionally in abdominal cavities ( Pfaffenberger and Valencia, 1988; Verster, 1969). Taenia serialis is prevalent in North America, Europe and Africa. However, there are also recent reports of T. serialis in rabbits from Iran and China ( Moshiri et al., 2018; Zhang et al., 2018). Furthermore, PCR confirmed T. serialis eggs in the faeces from 2 out of 1425 dogs from rural Australia ( Jenkins et al., 2014). Hence, it is not surprising that this parasite has been occasionally found in Australian ring-tailed possums ( Pseudocheirus peregrinus ) and in kangaroos ( Macropus fulginosus ) ( Dunsmore and Howkins, 1968; Hough, 2000).

In contrast to T. multiceps with a predominantly domestic life cycle, wildlife plays a more prominent role in T. serialis . Surveys in the USA showed high prevalence throughout the nation, e.g. 12% (429 dogs) in Arizona and New Mexico and overall 3–29% in definitive hosts ( Ing et al., 1998). With regard to intermediate hosts, 46% of 35 black-tailed jack rabbits ( Lepus californicus ) and 19% of a local rodent population were infected with T. serialis ( Pfaffenberger and Valencia, 1988; Schantz et al., 1977). Henke et al. (2002) reported on T. multiceps in coyotes ( C. latrans ) from Texas but a misdiagnosis with T. serialis is probable in the absence of molecular species confirmation. Correspondingly, a recent study from Edmonton ( Canada) found T. serialis in 13% out of 23 urban coyote carcasses ( Luong et al., 2018). Interestingly, T. serialis was also found in arctic foxes ( Vulpes lagopus ) from north-east Greenland, demonstrating the widespread occurrence of this parasite in wild carnivores and the importance of a wildlife-cycle ( Andreassen et al., 2017). In Europe, T. serialis occurs in regions where lagomorphs are present. In the UK, 0.3–0.6% of hunting dogs and 0.5% of 197 foxes from the same region have been found positive for T. serialis , respectively ( Jones and Walters, 1992 a, 1992b). Interestingly, T. multiceps was absent in the same fox population, despite being in a sheep raising region with observed cases of coenurosis. In Northern Ireland, up to 4% of the local fox population was infected with T. serialis ( Ross and Fairley, 1969) . On the European mainland, this cestode is rarely reported in foxes. Correspondingly, by examining large numbers of foxes from Germany, 0.15–2.3% of foxes were positive ( Loos-Frank and Zeyhle, 1982; Pfeiffer et al., 1997; Welzel et al., 1995). In wolves, however, reported infection rates were 2.1% of 47 and 8% of 50 wolves in Spain ( Segovia et al., 2001, 2003), 5.9% of 68 wolves in Portugal ( Guerra et al., 2013), and 1% of 102 wolves in Serbia ( Cirovic et al., 2015a). Hence, wolf migration might be a risk for the dissemination of T. serialis from the southern and eastern parts of Europe to new areas. In this sense, T. serialis was found in 1.1% of 447 golden jackals from Serbia, a species migrating into Central Europe ( Cirovic et al., 2015b). A survey in Germany could not find adult T. serialis in 84 badgers, 47 stone marten, and 387 cats ( Loos-Frank and Zeyhle, 1982).

Rare cases of coenurosis in cats caused by T. serialis , but not by T. multiceps have been reported ( Hayes and Creighton, 1978; Huss et al., 1994; Orioles et al., 2014; Slocombe et al., 1989; Smith et al., 1988). Correspondingly, T. serialis -coenurosis represents a zoonosis with 11 case reports found in literature (Supplemental Table 1). The predominant location of the coenuri was subcutaneously or intramuscularly on the trunk of the patient. While cerebral infections due to T. serialis have been reported in sheep (and cats), there are no such reported cases in humans. The lesions were presented as palpable swellings, which were usually painless. Where indicated, all patients recovered after surgical removal of the lesion.

Several cases of T. serialis coenurosis in non-human primates have been reported, in contrast to T. multiceps with only one discribed case with uncertain diagnosis ( Table 4). Unlike in humans, cerebral, intra-abdominal, intramuscular and subcutaneous infections have been observed. Interestingly, in a study between 1971 and 1972 in an Ethiopian national park, metacestodes of T. serialis have been identified morphologically in large visible subcutaneous swellings in 9.2% of 92 gelada baboons. In a follow-up study (1974–1975) observing the same animals, 10.6% were infected ( Dunbar, 1980). Forty years later (2011), 4.8% of 291 other gelada baboons living in the same park had visible swellings, and in some of them, T. serialis was molecularly confirmed ( Schneider-Crease et al., 2013). Unlike in other intermediate hosts, these visible asymmetric masses can grow very large in baboons (>16× 20cm) and may show ulcerations, disturbing the animals obtrusively ( Schneider-Crease et al., 2013; Schwartz, 1927). Potentially, these large lesions can develop over long time periods because of a long life span and a low predation rate of the infected animals. In fact, only 0.9% of juvenile baboons presented visible swellings, as compared to 9.9% of adults ( Schneider-Crease et al., 2013). In spite of an endemic infection of primates, there were no human case-reports from Ethiopia, relativizing the zoonotic risk of T. serialis . Noteworthy, in contrast to e.g. T. crassiceps cysticercosis with single subcutaenous locations, many cases of T. serialis -coenurosis show multiple lesions, indicating a peroral infection and systemic parasite dissemination.

3.2.4. ‘African-type’ coenuroses

Reported cases of soft-tissue coenuroses in Africa are considered to be caused by T. brauni and T. glomeratus (syn. T. glomerata ). Taenia brauni is a tropical tapeworm of Eastern and Northern Africa, Rwanda and the Democratic Republic of Congo, with a wild animal life cycle, including dog, fox, jackal and genet as definitive hosts and rodents such as the swamp rat, porcupine and gerbil as intermediate hosts ( Collomb et al., 2007; Fain, 1956; Vanderick et al., 1964). Coenuri in the brain only have been reported from rats (Rattus r. rattus ) and non-human primates ( Fain, 1956). Taenia glomeratus , which can be distinguished from T. serialis by careful morphological examination ( Clapham, 1940 a, 1940b), has only been reported from Nigeria and the Democratic Republic of Congo ( Morel, 1959; Turner and Leiper, 1919).

In humans, 27 cases of T. brauni and one case of T. glomeratus have been reported from Rwanda, Uganda, Nigeria, and Congo, based on morphological identification and geographical association (Supplemental Table 1). There is only one report in a non-human primate ( Cercopithecus mitis doggetti ) from Rwanda with cysts in the brain, heart and parotid gland ( Fain, 1956).

Overall, only limited information is available on these cestode species and any recent data is missing. It has to be considered that these species may be strains of T. serialis , based on the shared host range, tissue tropism, and clinical signs ( Loos-Frank, 2000; Morel, 1959). However, there is no genetic data on T. brauni and T. glomeratus , and only a small number of published sequences for T. multiceps and T. serialis , which impair epidemiological studies ( Collomb et al., 2007).