Janna M. Schurer

Tradition and transition: Parasitic zoonoses of people and animals in Alaska, northern Canada, and Greenland

Zoonotic parasites are important causes of endemic and emerging human disease in northern North America and Greenland (the North), where prevalence of some parasites is higher than in the general North American population. The North today is in transition, facing increased resource extraction, globalisation of trade and travel, and rapid and accelerating environmental change. This comprehensive review addresses the diversity, distribution, ecology, epidemiology, and significance of nine zoonotic parasites in animal and human populations in the North. Based on a qualitative risk assessment with criteria heavily weighted for human health, these zoonotic parasites are ranked, in the order of decreasing importance, as follows: Echinococcus multilocularis, Toxoplasma gondii, Trichinella and Giardia, Echinococcus granulosus/canadensis and Cryptosporidium, Toxocara, anisakid nematodes, and diphyllobothriid cestodes. Recent and future trends in the importance of these parasites for human health in the North are explored. For example, the incidence of human exposure to endemic helminth zoonoses (e.g. Diphyllobothrium, Trichinella, and Echinococcus) appears to be declining, while water-borne protozoans such as Giardia, Cryptosporidium, and Toxoplasma may be emerging causes of human disease in a warming North. Parasites that undergo temperature-dependent development in the environment (such as Toxoplasma, ascarid and anisakid nematodes, and diphyllobothriid cestodes) will likely undergo accelerated development in endemic areas and temperate-adapted strains/species will move north, resulting in faunal shifts. Food-borne pathogens (e.g. Trichinella, Toxoplasma, anisakid nematodes, and diphyllobothriid cestodes) may be increasingly important as animal products are exported from the North and tourists, workers, and domestic animals enter the North. Finally, key needs are identified to better assess and mitigate risks associated with zoonotic parasites, including enhanced surveillance in animals and people, detection methods, and delivery and evaluation of veterinary and public health services.

Echinococcus canadensis, E. borealis, and E. intermedius. What's in a name?

The phylogenetic relationships of the G6, G7, G8, and G10 genotypes of Echinococcus granulosus are well defined, but their taxonomic status is currently unresolved. We apply an evolutionary species concept to infer that the G6 and G7 genotypes represent a single species that is different to both the G8 and G10 genotypes, and that the G8 and G10 genotypes are also on different evolutionary trajectories and, therefore, should be regarded as separate species. The names Echinococcus intermedius, Echinococcus canadensis, and Echinococcus borealis have been previously proposed for these three taxa (G6/7, G10 and G8, respectively) and we argue that it may be appropriate to resurrect these names. The correct delimitation and formal recognition of species of Echinococcus may have important veterinary and public health consequences.

Echinococcus multilocularis and Echinococcus canadensis in wolves from western Canada

Echinococcus species are important parasites of wildlife, domestic animals and people worldwide; however, little is known about the prevalence, intensity and genetic diversity of Echinococcus tapeworms in Canadian wildlife. Echinococcus tapeworms were harvested from the intestines of 42% of 93 wolves (Canis lupus) from five sampling regions in the Northwest Territories, Manitoba and Saskatchewan, and visually identified to genus level by microscopic examination. Genetic characterization was successful for tapeworms from 30 wolves, and identified both Echinococcus canadensis and Echinococcus multilocularis in all sampling locations. Mixed infections of E. canadensis/E. multilocularis, as well as the G8/G10 genotypes of E. canadensis were observed. These findings suggest that wolves may be an important definitive host for both parasite species in western Canada. This represents the first report of wolves naturally infected with E. multilocularis in North America, and of wolves harbouring mixed infections with multiple species and genotypes of Echinococcus. These observations provide important information regarding the distribution and diversity of zoonotic species of Echinococcus in western North America, and may be of interest from public health and wildlife conservation perspectives.

Parasitic Zoonoses: One Health Surveillance in Northern Saskatchewan

We report the results of a joint human-animal health investigation in a Dene community in northern Saskatchewan, where residents harvest wildlife (including moose, bear, elk, and fish), live in close contact with free roaming dogs, and lack access to permanent veterinary services. Fecal analysis of owned and free-roaming dogs over two consecutive years (N = 92, 103) identified several parasites of public health concern, including Toxocara canis, Diphyllobothrium spp., Echinococcus/Taenia, Cryptosporidium spp. and Giardia spp. Administration of pyrantel pamoate to a subset of dogs (N = 122) in the community in the first year was followed by reduced shedding of T. canis and other roundworms in the second year, demonstrating the potential utility of canine de-worming as a public health intervention. Using direct agglutination tests with confirmatory indirect fluorescent antibody test, 21% of 47 dogs were sero-positive for exposure to Toxoplasma gondii. Using enzyme-linked immunosorbent assay (ELISA) sero-prevalence rates in 201 human volunteers were as follows: Toxoplasma gondii (14%), Echinococcus granulosus (48%), Toxocara canis (13%) and Trichinella spp. (16%). Overall 65% of participants were sero-positive for at least one parasite. A survey administered to volunteers indicated few associations between widely accepted risk factors for parasite exposure and serological status, emphasizing the importance of environmental transmission of these parasites through soil, food, and waterborne routes.

Surveillance for Echinococcus canadensis genotypes in Canadian ungulates

Graphical abstract Highlights ► 15 Echinococcus canadensis ungulate isolates were genetically characterized. ► Sequencing occurred at the NADH dehydrogenase subunit 1 (NAD1) mitochondrial gene. ► G10 genotypes detected in moose, elk, caribou; G8 genotype detected in muskox. ► The Canadian wildlife database (CCWHC) was searched for E. canadensis records. ► E. canadensis is present across Canada except the Atlantic provinces and High Arctic.

Sentinel Surveillance for Zoonotic Parasites in Companion Animals in Indigenous Communities of Saskatchewan

Indigenous communities may have increased risk of exposure to zoonotic parasites, including Echinococcus granulosus, Toxocara canis, Toxoplasma gondii, Diphyllobothrium spp., and Giardia duodenalis, for which dogs may serve as sentinels for or sources of human infection. Canid fecal samples were collected from dogs and the environment in five indigenous communities across Saskatchewan and Alberta (N = 58, 62, 43, 66, and 25). Parasites in individual fecal samples were quantified using fecal flotation and a commercial immunofluorescent antibody test for Giardia and Cryptosporidium. Overall, the prevalence of canine intestinal parasitic infection was 20-71%, which is 5-16 times higher in indigenous communities than a nearby urban center in Saskatchewan. The overall prevalences of T. canis, Diphyllobothrium, and taeniid eggs in dog feces were, respectively, 11.8%, 4.9%, and 1.2% in our study compared with 0-0.2% in urban dogs. Giardia cysts present in 21% of samples were identified as zoonotic genotype Assemblage A.

Unexpected diversity of the cestode Echinococcus multilocularis in wildlife in Canada

Echinococcus multilocularis is a zoonotic cestode with a distribution encompassing the northern hemisphere that causes alveolar hydatid disease in people and other aberrant hosts. E. multilocularis is not genetically uniform across its distribution, which may have implications for zoonotic transmission and pathogenicity. Recent findings of a European-type haplotype of E. multilocularis in wildlife in one location in western Canada motivated a broader survey of the diversity of this parasite in wildlife from northern and western Canada. We obtained intact adult cestodes of E. multilocularis from the intestines of 41 wild canids (wolf - Canis lupus, coyote - Canis latrans, and red fox - Vulpes vulpes), taeniid eggs from 28 fecal samples from Arctic fox (Vulpes lagopus), and alveolar hydatid cysts from 39 potential rodent intermediate hosts. Upon sequencing a 370-nucelotide region of the NADH dehydrogenase subunit 1 (nad1) mitochondrial locus, 17 new haplotypes were identified. This constitutes a much higher diversity than expected, as only two genotypes (European and an Asian/North American) had previously been identified using this locus. The European-type strain, recently introduced, may be widespread in wildlife within western Canada, possibly related to the large home ranges and wide dispersal range of wild canids. This study increased understanding of the biogeographic distribution, prevalence and genetic differences of a globally important pathogenic cestode in northern and western Canada.

People, Pets, and Parasites: One Health Surveillance in Southeastern Saskatchewan

Residents of remote and Indigenous communities might experience higher exposure to some zoonotic parasites than the general North American population. Human sero-surveillance conducted in two Saulteaux communities found 113 volunteers exposed as follows: Trichinella (2.7%), Toxocara canis (4.4%), Echinococcus (4.4%), and Toxoplasma gondii (1.8%). In dogs, 41% of 51 fecal samples were positive for at least one intestinal parasite, 3% of 77 were sero-positive for Borrelia burgdorferi, and 21% of 78 for T. gondii. Echinococcus exposure was more likely to occur in non-dog owners (odds ratio [OR]: 11.4, 95% confidence interval [CI]: 1.2-107, P = 0.03); while T. canis was more likely to occur in children (ages 4-17) (OR: 49, 95% CI: 3.9-624; P = 0.003), and those with a history of dog bites (OR: 13.5, 95% CI: 1.02-179; P = 0.048). Our results emphasize the use of dogs as sentinels for emerging pathogens such as Lyme disease, and the need for targeted surveillance and intervention programs tailored for parasite species, cultural groups, and communities.

Stabilizing Dog Populations and Improving Animal and Public Health Through a Participatory Approach in Indigenous Communities.

Free‐roaming dog populations are a global concern for animal and human health including transmission of infectious disease (e.g. rabies, distemper and parasites), dog bite injuries/mortalities, animal welfare and adverse effects on wildlife. In Saskatchewan (SK), Canada, veterinary care is difficult to access in the remote and sparsely inhabited northern half of the province, where the population is predominately Indigenous. Even where veterinary clinics are readily available, there are important barriers such as cost, lack of transportation, unique cultural perspectives on dog husbandry and perceived need for veterinary care. We report the effects of introducing a community action plan designed to improve animal and human health, increase animal health literacy and benefit community well‐being in two Indigenous communities where a dog‐related child fatality recently occurred. Initial door‐to‐door dog demographic surveys indicated that most dogs were sexually intact (92% of 382 dogs), and few had ever been vaccinated (6%) or dewormed (6%). Approximately three animal‐related injuries requiring medical care were reported in the communities per 1000 persons per year (95% CL: 1.6–6.6), and approximately 86% of 145 environmentally collected dog faecal samples contained parasites, far above levels reported in other urban or rural settings in SK. Following two subsidized spay/neuter clinics and active rehoming of dogs, parasite levels in dog faeces decreased significantly (P < 0.001), and important changes were observed in the dog demographic profile. This project demonstrates the importance of engaging people using familiar, local resources and taking a community specific approach. As well, it highlights the value of integrated, cross‐jurisdictional cooperation, utilizing the resources of university researchers, veterinary personnel, public health, environmental health and community‐based advocates to work together to solve complex issues in One Health. On‐going surveillance on dog bites, parasite levels and dog demographics are needed to measure the long‐term sustainability of benefits to dog, human and wildlife health.

Response to Nakao et al. – is Echinococcus intermedius a valid species?

The aim of our Opinion article [1] was to stimulate discussion on the taxonomic status of the G6, G7, G8, and G10 genotypes of Echinococcus granulosus, and we therefore welcome the letter from Nakao et al. (2015) [2]. They make two main points, one concerning the separation of the G8 and G10 (cervid) genotypes, and one concerning the nomenclature of the G6/G7 (camel and pig) genotypes. With both these points there are aspects which we can agree upon, but others about which we must disagree. However, the areas of disagreement can be settled empirically with further data, and we hope that such data will be forthcoming soon.