ECHINOCOCCUS MULTILOCULARIS

CAUSATIVE AGENT (CLASSIFICATION, morphology) Echinococcus multilocularis adults are small, only 1.2 to 3.7 mm long (Roberts and Janovy 2000). In contrast to E. granulosus, there is very little genetic varia­tion among the strains of E.

host range and distribution Echino­coccus multilocularis typically infects canids and felids as definitive hosts and various rodents, monkeys, and pigs as intermediate hosts (Thompson and McManus 2002). Distribu­tion is inconsistent, but covers parts of North America, western Europe, China, and Japan (Lucius and Bilger 1995).

Several regional cycles are documented (Thompson and McManus 2002). In continen­tal North America, one cycle involves red foxes (Vulpes vulpes), coyotes (Canis latrans), domestic dogs, and cats as definitive hosts; wild rodents (e.g., Microtus pennsylvanicus, Peromyscus man- iculatus) and house mice (Mus musculus) serve as intermediate hosts (Leiby et al. 1970). A cycle in Alaska involves foxes (Alopex lagopus, Vulpes vulpes) and a variety of rodents [e.g., Citellus (Spermophilus) spp., Clethrionomys spp., Lemmus spp., and Microtus spp.) (Rausch and Schiller 1951, Thomas et al. 1954). The Euro­pean, former USSR, and China cycle involves red foxes, wolves (Canis lupus), raccoon-dogs (Nyctereutes procyonoides), domestic dogs, and cats as definitive hosts, and a variety of rodents (e.g., Microtus spp., Apodemus spp., Arvi- cola terrestris, Clethrionomys glareolus, Ondatra zibethicus, Pitymys subterraneus, Myospalax fontainieri), wild pigs (Sus scrofa), monkeys, domestic pigs, and dogs as intermediate hosts (Lucius and Bilger 1995, Hofer et al.

life cycles and variations Adult ces- todes living in the small intestine of the defini­tive hosts shed eggs (Fig. 4.11) with the feces; eggs are highly resistant to environmental stresses (Thomas and Babero 1956). Following their ingestion by suitable intermediate hosts, oncospheres hatch in the stomach or small intestine, penetrate the mucosa, enter the circu­lation, and are carried to the liver (Rausch 1954, Leiby and Dyer 1971). With infections of longer duration, secondary foci in the spleen, mesen­tery, and peritoneum can develop after metas­tasis (Rausch 1954). Infection of the definitive host occurs by ingestion of the alveolar larvae, with the adult worms reaching maturity in 6 to 8 weeks (Leiby and Dyer 1971).

reservoirs and transmission Although prevalences of E. multilocularis typically are low, they can reach 50% or more among definitive hosts and 20% in intermediate hosts (Hofer et al. 2000). Infections in rodents reflect inherent susceptibility as well as variations in habitats, behaviors, and food habits. Deer mice (Peromyscus spp.) may have greater exposure to ova than other rodents in a habitat because they often live near abandoned fox dens and also scavenge feces (Leiby et al. 1970). Likewise, extent of ground cover and proximity to habi­tat edges can contribute to risk of infections (Leiby and Kritsky 1974, Delattre et al. 1990). Further, deer mice can acquire larval infections by ingesting terrestrial beetles exposed to fox feces (Leiby and Nickel 1968).

Habitat and soil type can be important. In France, the E. multilocularis life cycle was best completed on two types of beech forest-associated habitats (Gilot et al. 1988). In Germany, infected foxes were associated with bodies of water, high soil humidity, and on pastures, suggesting that the level of dry­ness was limiting to oncospheres and that open landscapes with humid soils were favor­able for the parasite; heavily forested areas had fewer infected foxes (Staubach et al.

CLINICAL EFFECTS AND IDENTIFICATION Definitive hosts rarely have clinical symptoms, even when infected with several thousand adult worms; this has included foxes infected with several hundred thousand adults (Leiby and Dyer 1971, Frank 1976). In contrast, intermedi­ate hosts can be severely affected by the hyda­tid. Hydatids are space filling, and brood cap­sules can bud out and grow into all openings of a tissue or organ. Under experimental con­ditions, the hydatids can greatly increase liver size and cause death among infected rodents (Frank 1976). In field mice with infections of long duration, the abdomen becomes greatly distended and movement is impaired (Leiby and Dyer 1971). Such intermediate hosts are more readily preyed upon by definitive hosts to complete the life cycle.

Identification of echinococcosis usually follows examination of the definitive hosts for adult worms at necropsy, or finding gravid seg­ments in feces (Leiby and Dyer 1971). Scraping, filtration, and counting is an effective and efficient method for finding and counting the parasites (Gesy et al. 2013). However, identifi­cation by PCR (Bowles and McManus 1993b), including for eggs (Mathis et al.

population effects Echinococcus mul- tilocularis rarely has adverse effects on defini­tive hosts, and there is no clear evidence for population impacts on intermediate hosts from E. multilocularis. Interestingly, the success of rabies control programs across Europe has led to increases in fox populations in France, Germany, and Switzerland (Artois 1997); this has coincided with increases in reported prevalences of E. multilocularis among foxes in southern Germany, Austria, and eastern France (Lucius and Bilger 1995, Giraudoux et al. 2001, Duscher et al. 2006).

special problems Humans can develop hydatid cysts after ingesting ova shed by defini­tive hosts. However, humans are dead-end intermediate hosts; the metacestode does not mature and remains in a proliferative stage indefinitely, thus continually invading and destroying hepatic and other infected tissue (Rausch and Wilson 1973). Many human infec­tions occur in childhood, but the rate of growth of the larvae is so slow that clinical signs do not usually become evident until much later (Fay 1973). In humans, metastasis to other organs is an additional problem for E. multi- locularis (Roberts and Janovy 2000). Human infections are hard to treat; surgical removal of the hydatid is dangerous because of the risk of rupture and anaphylaxis. Also, metastasis and formation of secondary cystic hydatid lesions makes it difficult to remove all hydatid material (Schantz et al. 1982).

There is a significant association between infected hosts with E. multilocularis and increased prevalences of human alveolar echi­nococcosis (Giraudoux et al. 2003). Yet high prevalences of E. multilocularis among defini­tive hosts and intermediate hosts in urban areas are not necessarily linked to increased cases of alveolar hydatid disease in humans (Hofer et al.

control and host immunity Strategies for control of E. multilocularis often depend on whether the pastoral (domestic dog) or sylvatic (wild fox) cycle is involved (Ito et al. 2003). Where domestic dogs are the principal hosts, strategies include reducing numbers of stray dogs, registration and preventive chemotherapy for owned dogs, and information campaigns outlining low-risk behaviors. With wild canids involved, integrative strategies may include campaigns with prevention information, restricting access of pet animals to rodents, chemotherapy of foxes on local or regional scales, and strategies to minimize human-fox contacts (Ito et al. 2003).

Praziquantel has been a drug of choice in control of this parasite (Bush et al. 2001). Praziquantel in baits reduced the prevalence of E. multilocularis among red foxes in Japan; prevalences among intermediate host voles also declined during this time (Tsukada et al. 2002). Similarly, praziquantel was use­ful for reducing E. multilocularis prevalences among red foxes of Switzerland (Hegglin and Deplazes 2008). However, in some species, praziquantel may enhance growth of alveolar hydatids (Marchiondo et al. 1994). Niclosamide is effective against Echinococcus spp. and other cestodes in naturally or experimentally infected wolves, foxes, jackals, hyenas, and dogs (Bekirov and Dzhumaev 1976). Albendazole is effective in some animals (Rodrigues et al. 1995).

Some vaccines are being developed for Echinococcus granulosus and Taenia solium for humans and some domestic animals (Lightowlers et al. 2000). However, none are yet available for E. multilocularis.