Echinococcus multilocularis in Urban Coyotes, Alberta, Canada

Echinococcus multilocularis is a zoonotic parasite in wild canids. We determined its frequency in urban coyotes (Canis latrans) in Alberta, Canada. We detected E. multilocularis in 23 of 91 coyotes in this region. This parasite is a public health concern throughout the Northern Hemisphere, partly because of increased urbanization of wild canids.

more abundant than foxes. E. multilocularis was reported in 7 (4.1%) of 171 coyotes in the northcentral United States in the late 1960s (3), and subsequently prevalences ranging from 19.0% to 35.0% have been reported in coyotes in the central United States (4).
In Canada, E. multilocularis was detected in 10 (23.0%) of 43 coyotes in Riding Mountain National Park, Manitoba (5). In Alberta, 1 case was recorded from the aspen parkland in 1973 (5) but it was not found in coyotes from forested regions and southern prairies (6,7). Nonetheless, E. multilocularis is generally considered enzootic to central and southern Alberta on the basis of its prevalence in rodent intermediate hosts. During the 1970s, sixty-three (22.3%) of 283 deer mice (Peromyscus maniculatus) trapped in periurban areas of Edmonton were positive for alveolar hydatid cysts (8), and E. multilocularis was also detected in 2 deer mice collected <1.8 km from Lethbridge in southern Alberta (9).
Because mice and voles (family Cricetidae, including Peromyscus spp.) have been reported as main prey (70.1%) of coyotes in Calgary (10), and coyotes are common in urban areas of Calgary and Edmonton, we suspected a role for this carnivore in the maintenance of the wild animal cycle of E. multilocularis in such urban settings. Thus, we aimed to ascertain the frequency of E. multilocularis in coyotes from metropolitan areas in Alberta, Canada.

The Study
Ninety-one hunted or road-killed coyotes were collected during October 2009-July 2011. Most (n = 83) of the carcasses were from the Calgary census metropolitan area (CMA) (Figure 1). The remainder (n = 8) were opportunistically collected from the Edmonton CMA. Of those from the Calgary CMA, the exact location of collection was known for 60 animals: 27 were from Calgary and 33 were from the rural fringe, including 2 near Strathmore. Of the carcasses from the Edmonton CMA, 7 were from Edmonton and 1 was from a periurban site. Sex and age of 90 of the coyotes were recorded.
Before necropsy, all carcasses were stored at −20°C. Gastrointestinal tracts collected at necropsy were refrozen at −80°C for 3-5 days to inactivate Echinococcus spp. eggs. Once thawed and dissected, intestinal contents were washed, cleared of debris, and passed through a sieve (500μm pores), and the material in the sieve was examined for Echinococcus spp.
Adult tapeworms were counted and identifi ed as E. multilocularis on the basis of morphologic features ( Figure  2). To confi rm morphologic identifi cation, PCR was performed by using species-specifi c primers (11). Briefl y, a representative adult worm from each positive animal was E. multilocularis intensity (number of cestodes per host) ranged from 1 to 1,400 (median 20.5). The frequency of infection was signifi cantly higher in male coyotes (n = 44, 34.19%) than in female coyotes (n = 46, 15.2%; χ 2 4.337, df 1, P exact = 0.05) ( Table). No difference was detected between 43 juvenile coyotes and 47 adult coyotes (Table).

Conclusions
We demonstrated that E. multilocularis is common in coyotes of metropolitan areas of Calgary and Edmonton, Alberta, Canada, including their urban cores. This fi nding might indicate an emerging phenomenon similar to that observed in Europe with infi ltration of urban centers by E. multilocularis caused by an increase in red foxes in cities such as Copenhagen, Geneva, and Zurich (2). In Alberta, this phenomenon may be caused by coyotes occupying the urban landscape or by city sprawl invading the natural habitats of coyotes. Our data suggest that E. multilocularis is enzootic in coyotes in Alberta and that perpetuation of the wild animal cycle of E. multilocularis within cities and surroundings and potential infection of domestic dogs may pose a zoonotic risk, as documented on Saint Lawrence Island, Alaska, and in China (2,12). With a considerable increase in domestic dog population of Calgary (32.1% increase since 2001, a total of 122,325 dogs in 2010; Animal and Bylaw Services Survey 2010, www.calgary.ca/CSPS/ABS/Pages/ home.aspx) and substantial human population growth (32.9% increase in Calgary since 1999; Statistics Canada, 2009, www.statcan.gc.ca/start-debut-eng.html), awareness is needed of potential transmission risks associated with changing city landscapes and E. multilocularis in the urban environment.
In Canada, only 1 autochthonous human case of alveolar echinococcosis has been reported in Manitoba (13). However, imported cases have been described. In Alberta, there are no known reports of alveolar echinococcosis. This fi nding may be caused by the long incubation time required for clinical manifestation in humans (12) or a strain of E. multilocularis with a low zoonotic potential. Although there is little evidence of human risk from the strain of E. multilocularis in central North America (14), a human case caused by this strain has been confi rmed (15).
Our fi nding of E. multilocularis in coyotes in urban regions in Alberta suggests that surveillance for this parasite should be increased in North America. Although removal of this parasite from domestic dogs and cats is effective, eradication from free-ranging defi nitive hosts may be unfeasible (2,12). Interventions other than improving public awareness about prevention and transmission risk are probably unnecessary, and public health messages should target veterinarians and dog owners because domestic dogs probably represent the main infection route for humans in North America (2,12). Genetic characterization of E. multilocularis and spatially explicit transmission models should also be developed to better assess risks of this emerging zoonosis in North America and worldwide.