Stacey A. Elmore

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.

Toxoplasma gondii in circumpolar people and wildlife.

Despite extensive worldwide surveillance in populations of both people and wildlife, relatively little is known about Toxoplasma gondii ecology in the circumpolar north. Many northern animals and people demonstrate exposure to T. gondii, but the apparent low densities of domestic or wild felids suggest that additional transmission mechanisms are responsible for T. gondii persistence in high latitudes, whether remote source (from another region), vertical, or dietary. People in these northern communities who practice subsistence hunting might have an increased infection risk due to traditional food preparation techniques and frequent handling of wild game. Recent advances in T. gondii genotyping, understanding of host-parasite relationships, and increased human and wildlife surveillance will help to address knowledge gaps about parasite evolution, distribution, and abundance throughout the Arctic and Subarctic.

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.

Endoparasites in the feces of arctic foxes in a terrestrial ecosystem in Canada

Graphical abstract

Toxoplasma gondii exposure in arctic-nesting geese: A multi-state occupancy framework and comparison of serological assays

Graphical abstract

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.

The role of European starlings in the spread of coccidia within concentrated animal feeding operations

To investigate the relationship between European starlings and bovine coccidiosis we collected samples from European starlings, cattle feed bunks, cattle water troughs, and cattle feces within concentrated animal feeding operations (CAFOs). These samples were screened for coccidia spp. to investigate (i) the prevalence of coccidia in starlings using CAFOs; (ii) if there is a relationship between bovine coccidiosis and starling numbers; (iii) if coccidia contamination of cattle feed and water is related to the number of starlings observed on CAFOs. Coccidia belonging to the genus Eimeria were detected in cattle feces and one water sample but no Eimeria spp. were detected in European starlings or cattle feed. However, many European starling samples were positive for Isospora. Starling use of CAFOs did not appear to be associated with coccidia spp. shedding by cattle and there was no correlation between starling numbers and contamination of cattle feed and water, suggesting that starling do not contribute to the amplification and spread of Eimeria in CAFOs.

Multi-scale occupancy approach to estimate Toxoplasma gondii prevalence and detection probability in tissues: an application and guide for field sampling.

Increasingly, birds are recognised as important hosts for the ubiquitous parasite Toxoplasma gondii, although little experimental evidence exists to determine which tissues should be tested to maximise the detection probability of T. gondii. Also, Arctic-nesting geese are suspected to be important sources of T. gondii in terrestrial Arctic ecosystems, but the parasite has not previously been reported in the tissues of these geese. Using a domestic goose model, we applied a multi-scale occupancy framework to demonstrate that the probability of detection of T. gondii was highest in the brain (0.689, 95% confidence interval=0.486, 0.839) and the heart (0.809, 95% confidence interval=0.693, 0.888). Inoculated geese had an estimated T. gondii infection probability of 0.849, (95% confidence interval=0.643, 0.946), highlighting uncertainty in the system, even under experimental conditions. Guided by these results, we tested the brains and hearts of wild Rosss Geese (Chen rossii, n=50) and Lesser Snow Geese (Chen caerulescens, n=50) from Karrak Lake, Nunavut, Canada. We detected 51 suspected positive tissue samples from 33 wild geese using real-time PCR with melt-curve analysis. The wild goose prevalence estimates generated by our multi-scale occupancy analysis were higher than the naïve estimates of prevalence, indicating that multiple PCR repetitions on the same organs and testing more than one organ could improve T. gondii detection. Genetic characterisation revealed Type III T. gondii alleles in six wild geese and Sarcocystis spp. in 25 samples. Our study demonstrates that Arctic nesting geese are capable of harbouring T. gondii in their tissues and could transport the parasite from their southern overwintering grounds into the Arctic region. We demonstrate how a multi-scale occupancy framework can be used in a domestic animal model to guide resource-limited sample collection and tissue analysis in wildlife. Secondly, we confirm the value of traditional occupancy in optimising T. gondii detection probability in tissue samples.

Vector-borne pathogens in arctic foxes, Vulpes lagopus, from Canada

Because of the relatively low biodiversity within arctic ecosystems, arctic foxes, Vulpes lagopus, could serve as sentinels for the study of changes in the ecology of vector-borne zoonotic pathogens. The objective of this study was to determine the molecular prevalence of 5 different genera of vector borne pathogens (Anaplasma, Babesia, Bartonella, Ehrlichia, and Hemotropic Mycoplasma spp.) using blood collected from 28 live-trapped arctic foxes from the region of Karrak Lake, Nunavut, Canada. Bartonella henselae (n = 3), Mycoplasma haemocanis (n = 1), Ehrlichia canis (n = 1), and an Anaplasma sp. (n = 1) DNA were PCR amplified and subsequently identified by sequencing. This study provides preliminary evidence that vector borne pathogens, not typically associated with the arctic ecosystem, exist at low levels in this arctic fox population, and that vector exposure, pathogen transmission dynamics, and changes in the geographic distribution of pathogens over time should be investigated in future studies.

ESTIMATING TOXOPLASMA GONDII EXPOSURE IN ARCTIC FOXES (VULPES LAGOPUS) WHILE NAVIGATING THE IMPERFECT WORLD OF WILDLIFE SEROLOGY

Abstract Although the protozoan parasite Toxoplasma gondii is ubiquitous in birds and mammals worldwide, the full suite of hosts and transmission routes is not completely understood, especially in the Arctic. Toxoplasma gondii occurrence in humans and wildlife can be high in Arctic regions, despite apparently limited opportunities for transmission of oocysts shed by felid definitive hosts. Arctic foxes (Vulpes lagopus) are under increasing anthropogenic and ecologic pressure, leading to population declines in parts of their range. Our understanding of T. gondii occurrence in arctic foxes is limited to only a few regions, but mortality events caused by this parasite have been reported. We investigated the exposure of arctic foxes to T. gondii in the Karrak Lake goose colony, Queen Maud Gulf Migratory Bird Sanctuary, Nunavut, Canada. Following an occupancy-modeling framework, we performed replicated antibody testing on serum samples by direct agglutination test (DAT), indirect fluorescent antibody test (IFAT), and an indirect enzyme-linked immunosorbent assay (ELISA) that can be used in multiple mammalian host species. As a metric of test performance, we then estimated the probability of detecting T. gondii antibodies for each of the tests. Occupancy estimates for T. gondii antibodies in arctic foxes under this framework were between 0.430 and 0.758. Detection probability was highest for IFAT (0.716) and lower for DAT (0.611) and ELISA (0.464), indicating that the test of choice for antibody detection in arctic foxes might be the IFAT. We document a new geographic record of T. gondii exposure in arctic foxes and demonstrate an emerging application of ecologic modeling techniques to account for imperfect performance of diagnostic tests in wildlife species.