tradition and transition

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From Jenkins, E.J., Castrodale, L.J., de Rosemond, S.J.C., Dixon, B.R., Elmore, S.A.,Gesy, K.M., Hoberg, E.P., Polley, L., Schurer, J.M., Simard, M., Thompson, R.C.A., 2013.

Tradition and Transition: Parasitic Zoonoses of People and Animals in Alaska, NorthernCanada, and Greenland. In: Rollinson, D. (Ed.), Advances in Parasitology, Academic Press,

pp. 33–204.ISBN: 9780124077065

Copyright © 2013 Elsevier Ltd. All rights reserved.Academic Press

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Advances in Parasitology, Volume 82 ISSN 0065-308X, http://dx.doi.org/10.1016/B978-0-12-407706-5.00002-2 33

© 2013 Elsevier Ltd.All rights reserved.

Advances in Parasitology, First Edition, 2013, 33-204

Our chapter is dedicated to Robert and Virginia Rausch, in every sense true pioneers of arctic parasitology and public health. We honour the memory of Robert Rausch, at his passing on 6 October 2012, for his insights and friendship spanning 70 years at the frontiers of northern science.

Contents1. Introduction 362. Methods 413. Giardia spp. 42

3.1. Species and Strains Present in the North 433.2. Geographic Distribution in the North 433.3. Transmission, Prevalence, and Animal Health Impact in the North 433.4. Transmission, Prevalence, and Public Health Impact in the North 513.5. Future Impact of Climate and Landscape Change 56

4. Cryptosporidium spp. 564.1. Species and Strains Present in the North 564.2. Geographic Distribution in the North 574.3. Transmission, Prevalence, and Animal Health Impact in the North 584.4. Transmission, Prevalence, and Public Health Impact in the North 624.5. Future Impact of Climate and Landscape Change 64

CHAPTER TWO

Tradition and Transition: Parasitic Zoonoses of People and Animals in Alaska, Northern Canada, and GreenlandEmily J. Jenkins*,1, Louisa J. Castrodale†, Simone J. C. de Rosemond*, Brent R. Dixon‡, Stacey A. Elmore*, Karen M. Gesy*, Eric P. Hoberg§, Lydden Polley*, Janna M. Schurer*, Manon Simard**, R. C. Andrew Thompson¶

*Department of Veterinary Microbiology, University of Saskatchewan, Saskatoon, SK S7N 5B4, Canada†Alaska Department of Health and Social Services, Division of Public Health, Section of Epidemiology, Anchorage, AK, USA‡Microbiology Research Division, Bureau of Microbial Hazards, Food Directorate, Health Canada, Ottawa, ON, Canada, K1A 0K9§United States National Parasite Collection, United States Department of Agriculture, Agricultural Research Service, Beltsville, MD, USA¶School of Veterinary and Biomedical Sciences, Murdoch University, Murdoch, WA, Australia**Nunavik Research Center, Makivik Corporation, Kuujjuaq, QC, Canada, J0M 1C01Corresponding author: E-mail: [email protected]


Emily J. Jenkins et al.34


5. Toxoplasma gondii 655.1. Species and Strains Present in the North 665.2. Geographic Distribution in the North 665.3. Transmission, Prevalence, and Animal Health Impact in the North 715.4. Transmission, Prevalence, and Public Health Impact in the North 73

5.4.1. Transmission 735.4.2. Prevalence 735.4.3. Risk Factors 735.4.4. Impact and Control 74

5.5. Future Impact of Climate and Landscape Change 755.5.1. Oocyst Transmission 755.5.2. Frequency and Severity of Waterborne Outbreaks 765.5.3. Abundance of and Access to Harvested Wildlife 76

6. Trichinella spp. 776.1. Species and Strains Present in the North 786.2. Geographic Distribution in the North 796.3. Transmission, Prevalence, and Animal Health Impact in the North 80

6.3.1. Transmission 806.3.2. Prevalence 826.3.3. Impact and Control in Animals 89

6.4. Transmission, Prevalence, and Public Health Impact in the North 896.4.1. Transmission and Risk Factors 896.4.2. Prevalence 936.4.3. Alaska 946.4.4. Canada 956.4.5. Greenland 976.4.6. Impact and Control in People 98

6.5. Future Impact of Climate and Landscape Change 1007. Toxocara spp. 102

7.1. Species Present in the North 1037.2. Geographic Distribution in the North 1047.3. Transmission, Prevalence, and Animal Health Impact in the North 1057.4. Transmission, Prevalence, and Public Health Impact in the North 1077.5. Future Impact of Climate and Landscape Change 109

8. Anisakid Nematodes 1118.1. Geographic Distribution in the North 1128.2. Species and Strains Present in the North 1128.3. Transmission, Prevalence, and Animal Health Impact in the North 1178.4. Transmission, Prevalence, and Public Health Impact in the North 1198.5. Future Impact of Climate and Landscape Change 120

9. Diphyllobothriid Cestodes 1219.1. Species Present in the North 1289.2. Geographic Distribution in the North 1299.3. Transmission, Prevalence, and Animal Health Impact in the North 131

9.3.1. Prevalence in Terrestrial Piscivores 1319.3.2. Prevalence in Marine Piscivores 135


Arctic Zoonoses 35


AbstractZoonotic parasites are important causes of endemic and emerging human disease in northern North America and Greenland (the North), where prevalence of some para-sites 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 multilocu-laris, 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

9.4. Transmission, Prevalence, and Public Health Impact in the North 1359.5. Diagnosis and Control 1409.6. Future Impact of Climate and Landscape Change 141

10. Echinococcus granulosus/canadensis (Cystic Hydatid) 14410.1. Species and Strains Present in the North 14410.2. Geographic Distribution in the North 14610.3. Transmission, Prevalence, and Animal Health Impact in the North 14710.4. Transmission, Prevalence, and Public Health Impact in the North 15010.5. Future Impact of Climate and Landscape Change 155

11. Echinococcus multilocularis (Alveolar Hydatid) 15711.1. Species and Strains Present in the North 15811.2. Geographic Distribution in the North 15911.3. Transmission, Prevalence, and Animal Health Impact in the North 16011.4. Transmission, Prevalence, and Public Health Impact in the North 16411.5. Future Impact of Climate and Landscape Change 166

12. Conclusions 16912.1. Zoonotic Parasites in the Traditional North 16912.2. Risk Assessment for Zoonotic Parasites in the North 17012.3. Risk Mitigation 17212.4. Zoonotic Parasites in a North in Transition 17312.5. Future Needs for Research and Surveillance of Zoonotic Parasites

in the North 175Acknowledgements 177References 177




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.

1. INTRODUCTION Worldwide, there is increasing recognition that zoonoses (especially those with wildlife reservoirs) are an important source of emerging dis-eases of people (Daszak et al., 2000; Kruse et al., 2004). Zoonoses are also ongoing contributors to health inequities; for example, 7 of 27 infectious diseases contributing significantly to the global Disability Adjusted Life Years burden were zoonotic, and 5 of these were parasitic (Robinson et al., 2003). Within the circumpolar north, there is increasing interest in priori-tising zoonotic diseases (including parasites) in terms of the current public health impact and predicting the effects of climate and landscape change on the ecology of these pathogens and their animal and human hosts in these vulnerable regions.

For purposes of this review, northern North America (‘the North’) was functionally defined as Alaska, Greenland, and northern Canada. In Canada, the North is functionally defined by the southern limit of the distribution of discontinuous permafrost (Fig. 2.1). This definition of North best reflects physical, cultural, and public health considerations and is more expansive than a strict definition of North as the Arctic (north of 60° of latitude). In total, the human population of the North (using this definition) is approxi-mately 2.5 million people in 8.5 million square kilometres. The population of Alaska is currently approximately 720,000 people, which represents <1% of the U.S. population. Of the total population of Alaska, 17% self-identify as indigenous (including Eskimo/Inuit, Aleut, Alaskan Athabaskan, Tlingit, Haida, and Tsimshian) (http://laborstats.alaska.gov/pop/estimates/pub/popover.pdf ). In Greenland, the total population is approximately 56,000 people, 85% of which are Inuit (Kalaallit), descended from the Thule migra-tion from Alaska and Canada in 800 A.C. (http://eu.nanoq.gl/emner/about%20greenland/facts%20on%20greenland.aspx). In Canada, the func-tional definition of the North corresponds well with health indicator peer groups E, F, and H as determined by Statistics Canada based on demographic


http://laborstats.alaska.gov/pop/estimates/pub/popover.pdf

http://laborstats.alaska.gov/pop/estimates/pub/popover.pdf

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http://eu.nanoq.gl/emner/about%20greenland/facts%20on%20greenland.aspx

Arctic Zoonoses 37


parameters and socioeconomic characteristics. These peer groups include the northern regions of the western provinces (British Columbia, Alberta, Saskatchewan, and Manitoba), the northern territories (Yukon, Northwest Territories, and Nunavut), northern Ontario, northern Quebec (Nunavik and the James Bay region), and Labrador. Collectively, the population in these peer groups is about 1.9 million people, representing 5.5% of the entire Canadian population, and is characterised by a high proportion of Indigenous people (First Nations, Metis, and Inuit) (http://www.statcan.gc.ca/pub/82-221-x/2011002/regions/hrt4-eng.htm). In Canada, Inuit living in Nunavut, Nunavik (in northern Quebec), and Nunatsiavut (in Labrador) represent 84–90% of the total population in these regions, and 55% of the population in the Inuvialuit region of the Northwest Territories. Based on 2006 census data, First Nations (primarily Cree, and Dene in

Figure 2.1 Functional de!nition of the North, including Greenland. Northern is con-sidered north of the line demarcating the southern limit of discontinuous permafrost (as low as 53°N in some regions). Abbreviations used in this !gure and throughout the review are as follows: Alaska (AK), United States of America (USA); provinces of Canada including British Columbia (BC), Alberta (AB), Saskatchewan (SK), Manitoba (MB), Ontario (ON), Quebec (QC) and Newfoundland Labrador (NL); territories of Canada including the Yukon Territory (YT), Northwest Territories (NT), and Nunavut (NU).


http://www.statcan.gc.ca/pub/82-221-x/2011002/regions/hrt4-eng.htm

http://www.statcan.gc.ca/pub/82-221-x/2011002/regions/hrt4-eng.htm



northwestern Canada) represent 76–97% of the population in northern Quebec ( James Bay), Saskatchewan, and Manitoba (http://www12.statcan.ca/census-recensement/2006/as-sa/97-558/index-eng.cfm). It is impor-tant to note that northern residents are a diverse population, and generalisa-tions about cultural and dietary preferences rarely apply from community to community, let alone across all of North America.

Northern peoples have had a long and continuous association with zoo-notic parasites, even prior to initial expansion into North America near the end of the Pleistocene (20–30,000 years ago). Subsequent parasite expo-sures were influenced by locally available food resources in aquatic and terrestrial environments (Hoberg et al., 2012). In current times, residents of northern and Indigenous communities in North America may be at higher risk of exposure to parasitic zoonoses than the general population. His-torically, prevalence of some zoonoses in northern residents has been dispa-rately higher than the North American average, suggesting increased risk of exposure resulting from a complex interaction of cultural, socioeconomic, and bioclimatic variables (Curtis et al., 1988; Fortuine, 1961; Gyorkos et al., 2003; Hotez, 2010). For example, cases of human cystic hydatid disease and Giardia have the highest per capita rates in northern Canadians (Gilbert et al., 2010; Public Health Agency of Canada, 2007). The seroprevalence of toxoplasmosis is as high as 60% in Nunavik Inuit, as compared to the overall North American estimate of 20% and a global prevalence of 30% ( Jones et al., 2001; Messier et al., 2009; Tenter et al., 2000).

Risk factors for transmission of zoonotic parasites in northern popula-tions include limited availability of veterinary and medical services, pres-ence of large free-roaming dog populations, and consumption of locally harvested fish and wildlife (Brook et al., 2010; Hotez, 2010; Salb et al., 2008). Inuit and other northern residents often hunt and butcher their own animals in the field or outside their home. Preferred species for harvest vary among communities; barren-ground caribou (Rangifer tarandus groenlandi-cus), marine mammals, and anadromous fish (e.g. char – Salvelinus alpinus, salmon – Onchorhynchus spp.) are mainstays of harvested wildlife among the Inuit, while in the sub-Arctic, moose (Alces alces), woodland caribou (R. t. caribou), and freshwater fish (e.g. grayling – Thymallus spp., whitefish – Coregonus spp.) dominate. Bears (Ursus spp.) and birds (e.g. sea ducks – Somateria spp., geese – Chen spp., ptarmigan – Lagopus spp.) are sometimes harvested, and furbearers (e.g. lynx – Lynx canadensis, fox – Vulpes spp., wolves – Canis lupus, wolverine – Gulo gulo) are still trapped, albeit in much fewer numbers than in the heyday of the fur trade (Mackey, 1988). Organs, meat,


http://www12.statcan.ca/census-recensement/2006/as-sa/97-558/index-eng.cfm

http://www12.statcan.ca/census-recensement/2006/as-sa/97-558/index-eng.cfm

Arctic Zoonoses 39


and fat are consumed fresh, thawed, frozen, partially cooked, fermented, dried, and cured as sausages. Some of these preparations can be a poten-tial risk for human health, linked to cases of trichinellosis, toxoplasmosis, diphyllobothriosis, and cystic hydatid disease (indirectly through dogs with access to carcasses of ungulates). Northern residents are also increasingly connected to the global food chain and in contact with transient work-forces and tourists, leading to adoption of dietary preferences from around the world that may not translate safely to local methods of food preparation (e.g. consuming raw pork or chicken) and to harvested foods (e.g. ceviche made with locally caught fish).

Northern residents are also at greater risk of water-borne infections. Water is generally brought to individual houses by truck. Although water quality is monitored and water is chlorine treated, chlorine does not kill protozoan parasites such as Giardia and Cryptosporidium, and water treatment infrastructure is often not optimal, with boil-water advisories issued to communities during spring run-off and heavy rainfalls. Chlorinated water is also unacceptable to some community members who continue to collect water from traditional sources (such as surface or rain water). Sewage is col-lected by truck from house tanks and held in an open pit away from com-munities. In some communities, wildlife are attracted to the sewage pits and have been observed drinking from them. In addition, during heavy rainfalls or ice thaws, sewage may overflow into surrounding groundwater. These infrastructure limitations may contribute to increased risk of transmission of parasitic zoonoses among people and wildlife in the Canadian North.

While risk factors for zoonoses in the North include traditional cultural practices of hunting, fishing and trapping, this must be weighed against the value of these activities and their palpable benefits for maintaining food secu-rity in remote and Indigenous communities (Chan et al., 2006; Lambden et al., 2007; Mackey, 1988; Ross et al., 1989). Indeed, zoonotic risks can be substantially reduced through a combination of protective traditional knowledge and modern food handling practices, as well as trends toward increased use of store-bought foods – truly a culture in transition.

Northern residents (Indigenous and others) may be at increased risk of exposure, and of developing disease, if zoonotic pathogens move north as a result of the rapidly changing Arctic climate. Dr. R. L. Rausch, the found-ing father of Arctic parasitology and to whom this review is dedicated, was prescient to draw attention to the commonalities of parasite transmission in northern and tropical regions, including relatively intact sylvatic cycles, introduction of pathogens with disastrous consequences, and socioeconomic




and ecological drivers of disease (Rausch, 1974). Indeed, he laid the founda-tions for anticipating that rapid and accelerating climate change might, in the course of a few decades, bring parasites historically restricted to temper-ate and tropical regions to the very threshold of the Arctic, where residents are largely naïve to these pathogens.

Forecasting the effects of ongoing climate and landscape change on transmission and impact of zoonotic parasites in the North is challenging because of the current lack of synthesised information about the diversity and distributions of parasites in these regions – a significant motivation for the current review. There is a wealth of information in older studies based on recovery of adult helminths from harvested animals; however, this review addresses an urgent need to update the current knowledge in light of new advances in molecular and immunological methods for detection and char-acterisation of helminth and protozoan parasites. From the animal health perspective, our knowledge of the distribution and abundance of parasites in animals in the North is often based on a few, dated studies in dogs and wildlife, and almost nothing is known about the impacts of parasitism on northern wildlife, especially at the population level. From a public health perspective, very few parasites in people are under surveillance (such as mandatory physician or laboratory reporting), and therefore cases are likely significantly underreported.

In addition, there is currently incomplete understanding of the local ecological drivers of transmission, as well as uncertainty in the magnitude of effects of climate change on temperature, precipitation, and habitat. How-ever, there no longer appears to be much controversy over the direction of climate change in the North, which is already moving into a warmer, wet-ter future, with increased frequency and severity of extreme weather events such as heavy rainfalls and storms. In marine systems, ocean temperatures are warming and record losses of sea ice are already observed (ACIA, 2005; Delecluse, 2008; Furgal and Prowse, 2008). Therefore, there is an urgent need to establish baselines for parasites of public and animal health sig-nificance against a future of climate, landscape, and cultural change in the North (Hoberg et al., 2012; Kutz et al., 2012).

This review considers the past, present, and future ecology of endopara-sitic zoonoses in animals, people, and the environment in the North Ameri-can Arctic – a ‘One-Health’ approach. The following zoonotic parasites are considered of ongoing and emerging importance in the North: pro-tozoans (Giardia, Cryptosporidium, and Toxoplasma), nematodes (Trichinella, Toxocara, and the zoonotic anisakids), and cestodes (diphyllobothriids and


Arctic Zoonoses 41


Echinococcus) (Curtis et al., 1988; Fortuine, 1961; Gyorkos et al., 2003; Hotez, 2010; Lantis, 1981; Rausch, 1972, 1974). For each parasite, we briefly review the biology, genetic diversity, host and geographic range, epidemiology and significance in both animals and people, and the potential impacts of envi-ronmental change on these vulnerable host–parasite systems in a North poised between tradition and transition.

2. METHODS The published literature was reviewed for each parasite as comprehensively as possible. Published studies (prevalence studies and case reports) for each parasite in animals and people in northern North America are summarised in tables. For maps, coordinates for the geographic loca-tions in the tables were obtained from the original publication. When this was not possible, we obtained coordinates for place names stated in the publications from GeoNames (http://www.geonames.org/), Canadian Geonames (http://www.nrcan.gc.ca/earth-sciences/geography-boundary/ geographical-name/search/5877), or Google Earth© (http://www.google.com/earth/index.html). All maps were created in ArcGIS© version 10. For studies where a pinpoint location was not available (i.e. reports covered a broad study area, or where communities were anonymised to protect pri-vacy), the centrum of the region was used. For some published data, it was simply not possible to find localising information. Therefore, all the points on the maps are derived from the corresponding tables, but not all data in the tables are represented in the maps.

In addition to the published literature, we drew on notifiable disease data for parasites (e.g. trichinellosis, giardiasis, and cryptosporidiosis) under passive surveillance in people through physician and laboratory reporting. Human cases summarised from passive surveillance data collected by public health authorities in Alaska and Canada were not mapped as the local-ising information was seldom available. These data were obtained from published sources, including the Canada Communicable Disease Report (http://www.phac-aspc.gc.ca/publicat/ccdr-rmtc/), National Notifiable Diseases Online (http://dsol-smed.phac-aspc.gc.ca/dsol-smed/ndis/list-eng.php), the Centers for Disease Control and Prevention Morbidity and Mortality Weekly Report (http://www.cdc.gov/mmwr/), and bulletins from the State of Alaska Health and Social Services (http://epi.alaska.gov/). Some of the Alaskan data were accessed through AK STARS, the State's reporting system for infectious diseases. Population data to calculate rates


http://www.geonames.org/

http://www.nrcan.gc.ca/earth-sciences/geography-boundary/geographical-name/search/5877

http://www.nrcan.gc.ca/earth-sciences/geography-boundary/geographical-name/search/5877

http://www.google.com/earth/index.html

http://www.google.com/earth/index.html

http://www.phac-aspc.gc.ca/publicat/ccdr-rmtc/

http://dsol-smed.phac-aspc.gc.ca/dsol-smed/ndis/list-eng.php

http://dsol-smed.phac-aspc.gc.ca/dsol-smed/ndis/list-eng.php

http://www.cdc.gov/mmwr/

http://epi.alaska.gov/



per 100,000 ! 2 people were obtained from the U.S. and Canadian census data available online. Cases (for those diseases with low incidence) and rates per 100,000 ! 2 people were graphed for each disease in order to demon-strate changes over multiyear periods with a relatively consistent detection effort. Laboratory methods no doubt changed over the reporting period (many decades in some cases); presumably this would bias toward increased detection as time progressed. Finally, some of the cases graphed may be duplicates of those reported in the tables.

3. GIARDIA SPP. The flagellate protozoan Giardia is one of the most common enteric parasites of people and domestic animals, and is increasingly recognised in a diverse range of wildlife species (Appelbee et al., 2005; Thompson et al., 2008, 2010). In the life cycle of Giardia, hosts become infected when cysts voided in faeces are ingested, which may be through direct host-to-host contact or via contaminated materials, water, food or arthropods (as mechanical vectors). Following ingestion, cysts break down in the duo-denum, where the trophozoites are released and subsequently proliferate asexually on the brush border villous epithelium of the mucosal surface (Thompson et al., 2008). Cysts released through the faeces are immediately infectious and remain infectious for months in water and cool, damp areas (Thompson et al., 2008).

An important aspect of the epidemiology of Giardia is understand-ing the host range of different species and strains/genotypes, how they are maintained in nature, and the potential for cross-transmission. This is particularly important in determining zoonotic potential, as Giardia can be maintained in a variety of transmission cycles that can operate inde-pendently (Hunter and Thompson, 2005). A large number of species and genotypes are now recognised that differ principally in their host range. Some species and genotypes appear to be restricted to particular species or types of hosts whereas others (the zoonotic assemblages) have broad host ranges including people. Giardia (previously known as Giardia lamblia and/or Giardia intestinalis) has been subdivided into seven Assemblages (A–H) or genotypes, now more appropriately designated with host-specific spe-cies names (Ballweber et al., 2010; Feng and Xiao, 2011; Lasek-Nesselquist et al., 2010; Thompson and Monis, 2012; Thompson et al., 2008). Thus, zoonotic assemblage A is now known as Giardia duodenalis, and zoonotic assemblage B as Giardia enterica.


Arctic Zoonoses 43


3.1. Species and Strains Present in the NorthAlthough few surveys have been undertaken in the North American Arc-tic on the genetic diversity and zoonotic significance of Giardia, zoonotic genotypes appear to be the only ones detected to date. Zoonotic genotypes A and B (G. duodenalis and G. enterica) have been reported in muskoxen in the western Canadian Arctic (Kutz et al., 2008), and G. duodenalis in dogs in the Northwest Territories, northern Alberta, and northern Saskatchewan (Himsworth et al., 2010b; Salb et al., 2008; Schurer et al., 2012). In the marine system, seals in the eastern Canadian Arctic were infected with G. enterica (Dixon et al., 2008). Further south, G. duodenalis has been reported in seals in the Gulf of St. Lawrence (Appelbee et al., 2010). One human isolate from a person in Alaska has been characterised as assemblage B (G. enterica), and is one of the first entire genomes of Giardia to have been char-acterised (Franzen et al., 2009). The presence of zoonotic assemblages A and B, which are the only two genotypes reported in people, and the absence of any animal host-specific genotypes, suggests that zoonotic transmission commonly occurs among people, dogs, and terrestrial and marine wildlife in the North American Arctic.

3.2. Geographic Distribution in the NorthGiardiasis is widespread in northern North America and Greenland (Fig. 2.2), and indeed a northern cline in prevalence has been noted ( Murphy, 1981). Cysts in faeces have been detected in people across northern North America at latitudes up to 69°N, and in animals as far north as 72°N (Tables 2.1 and 2.2). Giardia cysts have been found in drinking water and sewage effluent in the Yukon Territory (Roach et al., 1993) and in faecal samples from wildlife (Hueffer et al., 2011; Hughes-Hanks et al., 2005; Johnson et al., 2010; Kutz et al., 2008; Olson et al., 1997; Roach et al., 1993) and domestic animals (Bryan et al., 2011; Himsworth et al., 2010b) in various locations in northern Canada, Alaska, and Greenland (Fig. 2.2).

3.3. Transmission, Prevalence, and Animal Health Impact in the NorthGiardia cysts have been found in a number of domestic and wild animals in the North. Domestic dogs in northern communities have been shown to have unusually high prevalence of Giardia in faecal samples, with over half the dogs infected with zoonotic strains of Giardia in one Saskatchewan com-munity (Himsworth et al., 2010b), although prevalence was lower in other communities in northern SK (Schurer et al., 2012). Thus, a domestic animal




reservoir of human infection exists which will be an important consider-ation in control.

In the Yukon Territory, Canada, Giardia cysts were present in 14% of bea-ver samples and 25% of muskrat samples, as well as other terrestrial herbi-vore and carnivore species (Roach et al., 1993). Giardia infection in beavers (Castor canadensis) in North America has been linked to human outbreaks of Giardia infection for many years (Bemrick and Erlandsen, 1988; Davies and Hibler, 1979; Parkinson and Butler, 2005; Thompson et al., 1990). This was because of an association between cases of Giardia in campers who had drunk freshwater from streams in which infected beavers were found (Thompson et al., 2009). Subsequent studies have shown that beavers were unlikely to have been the original source, which was probably a contamina-tion event of human origin. However, the association was the prime reason for the World Health Organisation's recognition of the zoonotic potential of Giardia. Subsequent studies have also demonstrated that beavers are sus-ceptible to infection with zoonotic genotypes of Giardia with no evidence, to date, of a beaver adapted strain of Giardia (Thompson, 2011; Thompson et al., 2009).

Figure 2.2 Published reports of Giardia in animals and people in northern North America and Greenland. (Data from Tables 2.1 and 2.2).


Arctic Zoonoses45


Table 2.1 Prevalence [% (n)] of Giardia in Animals in Alaska, Northern Canada, and Greenland

Host LocationPrevalence [% (n)] Method References

Order Artiodactyla

Boreal Caribou (Rangifer tarandus caribou) Southwestern NT; Trout Lake 2 (149) SG-IFA Johnson et al. (2010)Dall's Sheep (Ovis dalli dalli) Southwestern YT 40 (5) SFI Roach et al. (1993)Muskoxen(Ovibos moschatus)

Sachs Harbour, Banks Island, NT

21 (72)*,† SG-IFA Kutz et al. (2008)

Order Carnivora

Dog (Canis familiaris) Villages, Kuskokwim River, AK <1 (234) MIF Fournelle et al. (1958)Camps, Kuskokwim River, AK 3.6 (55) MIF Fournelle et al. (1958)Hartley Bay, BC 40 (10) IFA Bryan et al. (2011)Fort Resolution, NT 8 (48)* SF Salb et al. (2008)Fort Chipewyan, AB 2 (48)* SF Salb et al. (2008)Northeastern SK 61 (155)* SG-IFA Himsworth et al. (2010b)Mamawetan Churchill River

region, SK21 (123)* SG-IFA Schurer et al. (2012)

Coyote (Canis latrans) Southwestern YT 67 (3) SFI Roach et al. (1993)Grizzly Bear (Ursus arctos) Southwestern YT 100 (3) SFI Roach et al. (1993)Wolf (Canis lupus) Southwestern YT 33 (3) SFI Roach et al. (1993)

Order Cetacea

Bowhead Whale (Balaena mysticetus) Barrow and Kaktovik, AK 33 (39) IFA Hughes-Hanks et al. (2005)North Atlantic Right Whale

(Eubalaena glacialis)Bay of Fundy, Canada/Cape

Cod, USA71 (49) IFA Hughes-Hanks et al. (2005)

Continued


Emily J. Jenkins et al.

46



Order Pinnipedia

Ringed Seal (Phoca hispida) Barrow, AK 65 (31) IFA Hughes-Hanks et al. (2005)Holman, NT 20 (15) SG-IFA Olson et al. (1997)Nunavik, QC 80 (55)† SG-IFA-

FCDixon et al. (2008)

Harp Seal (Phoca groenlandica) Magdalen Islands, Canada 50 (30) SG-IFA Measures and Olson (1999)Gulf of St. Lawrence, Canada 42 (38)* SG-IFA Appelbee et al. (2010)

Grey/Harbour Seal (Halichoerus grypus/Phoca vitulina)

Gulf of St. Lawrence/St. Lawrence Estuary, Canada

23 (22) SG-IFA Measures and Olson (1999)

Glacier Bay National Park, AK 6 (33) IFA Hueffer et al. (2011)Bearded Seal (Erignathus barbatus) Nunavik, QC 75 (4) SG-IFA-

FCDixon et al. (2008)

Hooded Seal (Cystophora cristata) Gulf of St. Lawrence, Canada 80 (10)* SG-IFA Appelbee et al. (2010)

Order Rodentia

Beaver (Castor canadensis) Southwestern YT 14 (14) SFI Roach et al. (1993)Muskrat (Ondatra zibethicus) Southwestern YT 25 (12) SFI Roach et al. (1993)

Phylum Mollusca

Blue Mussel (Mytilus edulis) Nunavik, QC 18 (11) IFA Lévesque et al. (2010)

Within a host species, reports move west to east. Abbreviations for states, provinces, and territories as in Fig. 2.1.SG-IFA – Sucrose gradient/immunofluorescent assay on faeces, SFI – Sucrose flotation, centrifugation, and iodine staining on faeces, MIF – Merthiolate iodine formalin faecal staining and concentration, IFA – Immunofluorescent assay on faeces, SF – Sucrose flotation and centrifugation on faeces, SG-IFA-FC – Sucrose gradient, immunofluorescent assay, and flow cytometry on intestinal contents, IFA – Immunofluorescent assay on pooled tissue.*Giardia duodenalis (Assemblage A).†Giardia enterica (Assemblage B).

Table 2.1 Prevalence [% (n)] of Giardia in Animals in Alaska, Northern Canada, and Greenland—cont’d


Arctic Zoonoses47


Table 2.2 Prevalence [% (n)] of Giardia in People in Alaska, Northern Canada, and Greenland Based on Published LiteratureLocation Sampling Dates Prevalence [% (n)] Method References

Alaska, USA

Bethel 1949 1 (100) ZCF Hitchcock (1950)Kotzebue 1950 1 (100) ZCF Hitchcock (1951)Kuskokwim River 1955–1956 2.3 (1261; in villages) 3.8

(419; in fishing camps)MIF Fournelle et al. (1958)

Kuskokwim River 1956–1957 6.3 (174) MIF Fournelle et al. (1959)Alaska, statewide 1969–1979 3.3 (10,618) (!66% from

northern AK)FFE Murphy (1981)

Juneau 1982 54 (24); plus 2 siblings NR Alaska Epi. Bull. (1982)*Ketchikan 1984 123 ill, 48 lab-confirmed NR Alaska Epi. Bull. (1984)†Statewide 1984–1985 198 cases NR Jenkerson and Middaugh (1987)Anchorage 1986 17 (35) IFA Alaska Epi. Bull. (1986)‡Anchorage 1986 8 (24) IFA Jenkerson and Middaugh (1987)Kodiak 1989 6 cases IFA Alaska Epi. Bull. (1990)**Hunting Lodge; NR 1990 18 cases NR Herwaldt et al. (1992)Juneau Falls, Kenai Peninsula 1991 13 (17) NR Alaska Epi. Bull. (1991)§Not stated 1995 10 cases NR Centers for Disease Control¶

Canada

Fort Chipewyan, AB 1945 14 (140) FS Saunders (1949)Southampton Island, NU 1947 3 (31) FE Brown et al. (1948)Igloolik, NU 1949 2 (97); Ages 1–4 years old FE Brown et al. (1950)Fort Chimo (Kuujjuaq), QC 1959 11 (46) Ages 0–9 years old FES Laird and Meerovitch (1961)

Continued



48


Location Sampling Dates Prevalence [% (n)] Method References

Hall Beach, NU 1970–1971 29 (105) FES Freeman and Jamieson (1976)Igloolik, NU 1970–1971 12 (247) FES Freeman and Jamieson (1976)12 communities; Sioux Lookout, ON

1974–1975 8.6 (536); Highest in ages 1–10 years old

FES Watson et al. (1979)

Arctic Bay, NU 1976 17 (153) NR Eaton (1976)8 communities; James Bay,

QC1982 5.8 (382); Highest in ages 1–9

years oldFES Brassard et al. (1985)

Greenland

Egedesminde and outposts 1957 7 (663); Highest in ages 0–4 (21%) and 5–14 (10%) years old

FES Babbott et al. (1961)

Abbreviations for states, provinces, and territories as in Fig. 2.1.ZCF – Zinc sulphate centrifugal flotation and iodine smear on faeces, MIF – Merthiolate iodine formalin staining and concentration on faeces, FFE – Faecal formal-ether, NR – Not recorded, IFA – Immunofluorescent assay on faeces, FS – Faecal smear, FE – Faecal examination, FES – Formalin–ether sedimentation on faeces.*http://epi.alaska.gov/bulletins/docs/b1982_21.htm.†http://epi.alaska.gov/bulletins/docs/b1984_20.pdf.‡http://epi.alaska.gov/bulletins/docs/b1986_08.htm.**http://epi.alaska.gov/bulletins/docs/b1990_04.htm.§http://epi.alaska.gov/bulletins/docs/b1991_27.htm.¶http://www.cdc.gov/Mmwr/preview/mmwrhtml/00055820.htm.

Table 2.2 Prevalence [% (n)] of Giardia in People in Alaska, Northern Canada, and Greenland Based on Published Literature—cont’d


http://epi.alaska.gov/bulletins/docs/b1982_21.htm

http://epi.alaska.gov/bulletins/docs/b1984_20.pdf




http://www.cdc.gov/Mmwr/preview/mmwrhtml/00055820.htm

Arctic Zoonoses 49


In other northern terrestrial wildlife, Giardia cysts have been found in faecal samples collected from boreal caribou (R. t. caribou) in northern Alberta, northern British Columbia, and southern Northwest Territories ( Johnson et al., 2010). Giardia cysts have also been found in faecal samples of Canada geese (Branta canadensis) residing in Maryland, USA (Graczyk et al., 1998). This indicates that Giardia may be present in winter-feeding grounds of migratory birds, which, when nesting in the Arctic in the summer, may serve as a potential source of infection for both wildlife and people (Grac-zyk et al., 2008).

People may be a source of infection for animals in some areas of north-ern Canada. Muskoxen (Ovibos moschatus) are indigenous to remote regions of the arctic tundra of Canada and Greenland. Giardia was first found in muskoxen in the Canadian Arctic in 1994, on Banks Island, and subse-quently proved to have a prevalence of 21% (Kutz et al., 2008, 2009b). Genotyping has demonstrated that the muskoxen harbour zoonotic strains of Giardia (assemblages A and B) (Kutz et al., 2008, 2009b). This has raised many interesting questions regarding the origin and epidemiology of this parasite in people and wildlife in this Arctic ecosystem. In particular, did people introduce Giardia and contaminate the ecosystem shared with mus-koxen? Is it now maintained in a sylvatic cycle involving muskoxen and possibly cervids, and thus a wildlife reservoir of human infection has now been established? The impact of infection on muskoxen is not understood, either in terms of muskoxen being a naïve host for Giardia, and the con-sequences of coinfection with other enteric parasites (Kutz et al., 2008, 2009b). It is known that Giardia occurs in the human population of Banks Island but there have been no molecular epidemiological surveys that could link human infections of Giardia with those in muskoxen (Hotez, 2010; Kutz et al., 2009b).

A number of recent studies have reported G. duodenalis in marine wild-life, particularly marine mammals and bivalve molluscs. In the marine environment, Giardia cysts have been reported in seawater in a number of studies, with the most likely source of contamination being sewage efflu-ent and surface run-off (Appelbee et al., 2005; Robertson, 2007). However, given the high prevalence of infection in some regions and the absence of agricultural run-off, marine mammals themselves may contribute sub-stantially to the contamination of the Arctic marine environment. Due to migration patterns, some Arctic seals and whales may also become exposed to Giardia in sub-Arctic and temperate marine environments, where human sewage and agricultural run-off are more common.




The majority of prevalence studies on Arctic marine wildlife have been done on seals. Moving from west to east, a relatively high prevalence of Giar-dia spp. (64.5%) was found in faeces of 31 ringed seals (Phoca hispida) (but not bearded seals – Erignathus barbatus) from Alaska (Hughes-Hanks et al., 2005), but only 6% of 33 harbour seals (Phoca vitulina) from Glacier Bay National Park, AK were infected (Hueffer et al., 2011). Olson et al. (1997) reported the presence of Giardia sp. cysts in 20% of ringed seals in Holman, NT in the western Canadian Arctic; however, Giardia was not detected in faecal samples collected from ringed seals from Shingle Point, YT. In the Gulf of St. Lawrence, Canada, G. duodenalis was identified in 42% of adult harp seals (Phoca groenlandica, syn. Pagophilus groenlandicus) and 80% of adult hooded seals (Cystophora cristata) (Appelbee et al., 2010). In Nunavik, QC, G. duodenalis was found in the gastrointestinal tract (GIT) of 80% of ringed seals and 75% bearded seals, which were collected for food by five different northern communities: Kangiqsujuaq, Quanqtaq, Kangiqsualujjuaq, Kuujj-uaq, and Inukjuak (Dixon et al., 2008). Giardia sp. cysts were also reported in the faeces of harp seals (50%), grey seals (23%), and a harbour seal from the east coast of Canada (Measures and Olson, 1999).

Other than seals, only a few other northern marine mammals have been reported as hosts for G. duodenalis. Giardia has been found in 33.3% of bowhead whales (Balaena mysticetus) residing off the coast of Alaska, USA (Hughes-Hanks et al., 2005). Giardia was not detected in beluga whales (Delphinapterus leucas) in Alaska or in the western Canadian Arctic (Hughes-Hanks et al., 2005; Olson et al., 1997). Similarly, on the east coast of Canada, beluga whales and a northern bottle-nosed whale were all negative for Giardia sp. cysts (Measures and Olson, 1999). However, further south, a very high prevalence (71.4%) of Giardia spp. was found in North Atlantic right whales from the Bay of Fundy, Canada, and Cape Cod, Massachusetts (Hughes-Hanks et al., 2005).

Giardia has been reported worldwide in a variety of bivalve molluscs (Fayer et al., 2004; Robertson, 2007). Viable Giardia cysts have also been identified in seawater (Robertson, 2007) and, as filter feeders, shellfish can filter large volumes of seawater, thereby concentrating the cysts in their tissues. There is very little information available, however, concerning the prevalence of Giardia in shellfish harvested in the Arctic. Giardia was reported in 18% of pooled samples of blue mussels collected in Nunavik, Quebec (Lévesque et al., 2010). The inclusion of shellfish in the diet of some seals, such as bearded seals, suggests this may be a potential source of infection in these animals.


Arctic Zoonoses 51


The impact of giardiasis on northern animal populations, especially wildlife, is unknown. Giardiasis can be clinically significant in people, young livestock, and young companion animals. In young livestock, Giardia infec-tions may adversely impact production (Olson et al., 2004; Thompson et al., 2008).

3.4. Transmission, Prevalence, and Public Health Impact in the NorthCases of Giardia in people are attributed to one of the two zoonotic geno-types/species (A or B/G. duodenalis and G. enterica); however, there is a great need for molecular epidemiological investigations to determine whether the source of infection for human cases and outbreaks is other people or animals (Porter et al., 2011). Giardia is most common in situations that support a high frequency of transmission, usually as a result of environ-mental contamination. Poor hygiene and inadequate sanitation are crucial factors in enhancing transmission of Giardia, exacerbated through contact with animal reservoirs (Thompson, 2011). Although the incidence of giar-diasis in people in the Arctic is not known, as with other parts of the world, disadvantaged Indigenous communities will be at greatest risk (Hotez, 2010; Kutz et al., 2009b).

Giardia is often transmitted through water and there is a clear associa-tion between contamination of drinking water and Giardia-infected animals and people residing within a watershed. The source of contamination is not always zoonotic strains of animal origin; indeed, genotyping procedures have often incriminated human effluent as the source of Giardia contamination of watersheds (Hunter and Thompson, 2005). In Canada, Giardia has been reported to be one of the leading causes of waterborne infections in people and was responsible for 47% of all waterborne disease outbreaks that occurred from 1974 to 2001 (Schuster et al., 2005). Furthermore, Wallis et al., 1996 analysed water samples collected from 72 municipalities across Canada and found that 73% of the raw sewage samples, 21% of the raw water samples, and 18% of the treated water samples contained Giardia cysts. In the Yukon, water from 32% of 22 pristine sites and 17% of 42 sites in Whitehorse (an urban region) were positive for Giardia cysts (Roach et al., 1993). According to Hunter and Thompson (2005), zoonotic transmission of Giardia between animals and people as a result of direct contact is considered rare; however, increasing recognition of zoonotic genotypes in dogs closely associated with human populations in northern Canada and elsewhere (Himsworth et al., 2010b; Salb et al., 2008; Schurer et al., 2012; Thompson, 2011) suggests




some mechanism of transmission, be it direct contact or through shared contaminated environments, food, or water.

In the North, food-borne routes may be an important type of zoonotic transmission of Giardia, especially for residents who consume raw shellfish, meat, and organs from harvested wildlife (Dixon et al., 2008; Hotez, 2010). There is potential for transmission through the consumption of raw meat or shellfish that have been contaminated with Giardia cysts of human or animal origin. A number of marine mammal species represent important food sources for the Inuit in Nunavik, Quebec (Ross et al., 1989), and elsewhere. It has been suggested that the consumption of marine mam-mals such as ringed seals, harp seals, and beluga may pose health risks due to zoonotic parasites, and that hunters, biologists, and veterinarians could also be at risk (Measures and Olson, 1999; Olson et al., 1997). The recent reports of zoonotic genotypes and species of Giardia in seals support these conclusions. For example, dried ringed-seal intestine is consumed widely in Nunavik and it is feasible, therefore, that this practice could contribute to the sporadic occurrence of giardiasis reported among the Inuit in the region (Hodgins, 1997). Contamination of seal meat with intestinal contents is also possible during the butchering process, and consumption of contaminated raw or aged seal meat is, therefore, another potential transmission route for Giardia in the North.

There is little evidence in the literature regarding outbreaks of giardiasis in northern communities, which suggests that asymptomatic infections are the norm, and/or that detection is suboptimal. Giardia is a common cause of diarrhoeal disease, and chronic infections among disadvantaged groups contribute to poor growth and other nutritional disorders, particularly in children (Thompson and Monis, 2011). Giardia may be a relatively com-mon cause of diarrhoeic illness in northern communities, where physicians presumptively treat with metronidazole (Roach et al., 1993). It is difficult to assess trends over time given the variety of laboratory techniques employed to detect Giardia. In Igloolik, NU, prevalence increased from 2% in 1949 to 12% in 1970–71, but this may reflect a more sensitive method of detec-tion. In Alaska, the number of Giardia isolations from samples submitted by physicians to the state public health laboratories increased over a 10-year period between 1969 and 1979 (Murphy, 1981). In Alaska, seasonal peaks in human infection were noted in fall (September–October), and the majority of clinical cases were people who had consumed or used untreated surface water while travelling within Alaska in the preceding two months (Murphy, 1981). In several studies, prevalence was highest in children less than 10


Arctic Zoonoses 53


years of age (Table 2.2), and in people in contact with young children and/or children in daycare centres (Jenkerson and Middaugh, 1990).

In Canada, giardiasis is a nationally notifiable communicable disease, and laboratory surveillance data are available from 1989 to 2008. Overall, cases per 100,000 people are declining Canada-wide. However, residents of the three northern territories of Canada still have a higher per capita rate of giardiasis than the Canadian average (Fig. 2.3). In the Yukon, per capita infec-tion was on average 3.4 (1.5–6) times higher than the Canada-wide average, while results were more variable for the Northwest Territories (mean 1.4 times higher, range 0.3–2.2) and Nunavut (mean 2.3, 0.5–5.5). Only nine years of data were available for Nunavut, Canada's newest northern terri-tory; prior to 2000, data from this region were included in the NT. Over a five year period (2002–2006), the mean annual number of isolations of enteric protozoa per 100,000 population was 35 for NU and 39 for the YT, more than double the Canada-wide average of 17 (Public Health Agency of

Figure 2.3 Passive surveillance for Giardia in people in the Yukon Territory (YT), North-west Territory (NT), Nunavut (NU), and Canada-wide, 1989–2008. [Data from the Noti!-able Diseases Online Database of the Public Health Agency of Canada (http://dsol-smed.phac-aspc.gc.ca/dsol-smed/ndis/index-eng.php) and the Canadian Noti!able Disease Surveillance System National Report: 2005–2008].


http://dsol-smed.phac-aspc.gc.ca/dsol-smed/ndis/index-eng.php




Canada, 2007). Of all reported enteric protozoal isolates in Canada in this time period, 73% were Giardia, 13% were Cryptosporidium, 12% were Ent-amoeba, and 3% were Cyclospora. Given a population of 30,000 in the Yukon in 2006, and 29,000 in Nunavut, there would have been approximately nine cases of giardiasis detected per year in YT and seven cases per year in NU (number of cases of enteric protozoans ! 0.73). Using underdiagnosis and reporting multipliers of 46.3 and 1.3 from the U.S. national data (Scallan et al., 2011), this suggests a total of 542 cases of giardiasis per year in YT, and 421 cases per year in NU. The underdiagnosis modifier may even be higher in the North, where both social and physical barriers can limit access to health care for residents, and clinicians may opt to treat presumptively given decreased access to diagnostic laboratories.

In Alaska, giardiasis is also a nationally notifiable communicable disease, and laboratory surveillance data are available from 1992 to 2010 (Fig. 2.4).

Figure 2.4 Passive surveillance for Giardia in people in Alaska (AK) and nationally for the United States of America, 1992–2010. (Data from the U.S. Centers for Disease Control Mor-bidity and Mortality Weekly Report Surveillance Summaries, http://www.cdc.gov/healthy-water/statistics/surveillance/health_data.html#giardia. Rates calculated for 1992–1997 using population estimates from http://www.census.gov/popest/data/historical/1990s/ and http://epi.alaska.gov/bulletins/docs/b1996_03.htm).


http://www.cdc.gov/healthywater/statistics/surveillance/health_data.html#giardia


http://www.census.gov/popest/data/historical/1990s/


Arctic Zoonoses 55


Since 1994, cases of giardiasis per 100,000 people have consistently been higher in Alaska (mean 1.9 times greater, range 1.3–2.8) than nationally in the USA. Between 2009 and 2010, the average annual incidence in Alaska (15.9 and 13.7 cases/100,000 population) was almost double the U.S. aver-age (7.3 and 7.8 cases/100,000 people) over this two-year time period (Yoder et al., 2010b). Giardia incidence therefore shows a northern cline on the North American continent, although this is not apparent within Alaska itself when regions are compared (Fig. 2.5). Giardia is the most com-mon cause of enteric illness in Alaska (Porter et al., 2011), and is the most significant enteric protozoan in the entire North American Arctic.

A variety of drugs are available to treat infections with Giardia in humans. However, it has been shown that therapeutic intervention is unlikely to have any long-term benefits in endemic, community situations where the frequency of reinfection is high because of environmental contamination and poor hygiene conditions. For example, a sustained, community-based control programme that used a regular 5-day treatment regimen of 400 mg albendazole, an effective antigiardial treatment, over 6.5 years in an isolated community effectively controlled coinfections with hookworm (Ancylos-toma duodenalis) but had no sustained effect on the prevalence of Giardia (Reynoldson et al., 1998; Thompson et al., 2001). Although Giardia was

Figure 2.5 Cases of giardiasis in people in Alaska by region, 1986–2010, as reported to the State Health Department. 5 year rates calculated with the mid-year population estimate. (Map from http://epi.alaska.gov/bulletins/docs/b1996_03.htm). (For colour version of this !gure, the reader is referred to the online version of this book.)





well suppressed by multiple doses of albendazole, regular six-monthly single doses of albendazole did not suppress the parasite in the long term. Rein-fection rates with Giardia by the faecal-oral route are rapid in such environ-ments in which cyst survival is possible, negating any transient benefits of chemotherapy without concurrent behavioural changes (Thompson, 2011; Thompson et al., 2001). Mass treatment must be combined with appropri-ate education programmes designed to prevent re-infection ( Savioli et al., 2006; Thompson et al., 2001).

3.5. Future Impact of Climate and Landscape ChangeGiardia is currently well-established in harsh northern climates, where cooler, wetter conditions favour survival and transmission of cysts. It is pos-sible that warming temperatures will decrease environmental survival of Giardia cysts. However, this will likely be offset by increased transmission through changes in regional hydrology.

Among the abiotic ecosystem components, water is the most important in terms of the impact of climate change (Polley and Thompson, 2009). Climate-induced rises in temperature will affect Arctic regions earlier and more severely than elsewhere given the diversity of water sources and this will clearly enhance opportunities for waterborne transmission of Giardia (Davidson et al., 2011). Climate change has long been predicted to increase the public health impacts of Giardia in the Arctic as a result of flooding events caused by heavy rain, snowfall, and melting, leading to outbreaks of waterborne infections (Parkinson and Butler, 2005).

Increased precipitation and frequency of severe weather events could overwhelm existing water treatment infrastructure, with a corresponding increase in the frequency and severity of waterborne outbreaks. Giardia is the most common cause of drinking water outbreaks in North America, likely as a result of the resistance of the cysts to chlorine treatment. Water treatment infrastructure in northern communities that does not involve fil-tration or ozonation should be considered vulnerable under current and future environmental conditions.

4. CRYPTOSPORIDIUM SPP.

4.1. Species and Strains Present in the NorthCryptosporidium is a protozoan parasite, associated with enteric disease in people and animals worldwide. The life cycle of Cryptosporidium includes asexual phases of proliferation on the mucosal surface, as well as epicellular


Arctic Zoonoses 57


proliferation and a sexual phase of reproduction. Infective oocysts are released in the faeces and are capable of prolonged survival in the environment (Hunter and Thompson, 2005). Re-infection is achieved when the oocysts are ingested; it is also possible for hosts to become superinfected when thin-walled cysts rupture inside the intestinal tract.

There are at least 19 different species and over 40 genotypes of Cryp-tosporidium (Elwin et al., 2012; Fayer, 2010; Xiao and Fayer, 2008), many of which are host-specific. For example, dogs are often infected with C. canis and cats with C. felis; however, despite widespread contact between people and pets, there appears to be limited transmission of these Cryp-tosporidium species to immunocompetent people (Xiao and Fayer, 2008). The zoonotic species Cryptosporidium parvum is the most widely distrib-uted, has the broadest host range, and is the species most commonly asso-ciated with human and livestock infections (Thompson and Smith, 2011; Xiao et al., 2004). According to Thompson and Smith (2011), livestock are the main reservoirs of zoonotic Cryptosporidium and may transmit this parasite to people via contaminated water or through direct contact. The absence of significant livestock populations may in part account for the apparently low prevalence of Cryptosporidium in arctic wildlife and peo-ple. However, many parasite studies in Arctic hosts have historically been based on faecal surveys using flotation techniques optimised for eggs of helminth parasites, and may be less sensitive for detecting the small oocysts of Cryptosporidium.

As a result, very little is known about the species or genotypes of Cryp-tosporidium present in the North. A distinct genotype related to Cryptospo-ridium muris, Cryptosporidium andersoni, and Cryptosporidium serpentis has been described in barren-ground caribou in the North Slope region of Alaska (Siefker et al., 2002). Santín et al., (2005) identified Cryptosporidium isolates from ringed seals in Nunavik, Quebec as C. muris, as well as two novel seal genotypes. Cryptosporidium oocysts recovered from blue mussels in Nunavik, Quebec, were morphologically similar to those of C. muris (Lévesque et al., 2010). The presence of C. muris is of concern with respect to public health as this species has been reported in immunocompetent people in a number of countries around the world (Xiao and Feng, 2008).

4.2. Geographic Distribution in the NorthCryptosporidiosis seems to be relatively uncommon in the North and has not to our knowledge been reported in animals or people in Greenland, although there have been few studies using methods that would detect this




parasite. In North America, Cryptosporidium oocysts have been detected in marine animals as far north as 71°N, and in shellfish, water, and faeces of terrestrial animals as far north as 61°N (Table 2.3; Fig. 2.6). Whether this represents a true northern distributional limit is questionable in light of the limited opportunities for detection. That said, several studies using sensitive detection methods have found Giardia but not Cryptosporidium in terrestrial and marine Arctic animals (Tables 2.1 and 2.3).

Cryptosporidium oocysts have been found in faecal samples or intesti-nal contents collected from terrestrial wildlife (Johnson et al., 2010; Roach et al., 1993) and domestic dogs in sub-Arctic regions of western Canada (Bryan et al., 2011; Himsworth et al., 2010b; Schurer et al., 2012), and in marine mammals and shellfish from Arctic waters (Dixon et al., 2008; Hughes-Hanks, 2005; Lévesque et al., 2010). Cryptosporidium oocysts have also been found in 5% of 42 water samples from Whitehorse and 14% of 11 raw water samples collected elsewhere in the Yukon Territory (Roach et al., 1993).

4.3. Transmission, Prevalence, and Animal Health Impact in the NorthAlthough Cryptosporidium has been found in multiple species in north-ern Canada, the prevalence of this protozoan in terrestrial animals was relatively low or, in some areas, the parasite was not detected at all (in comparable studies looking at the prevalence of Giardia). Prevalence in terrestrial ungulates was less than 2% in boreal caribou (R. tarandus cari-bou) in sub-Arctic Canada and 6% in barren-ground caribou (R. tarandus groenlandicus) in northwestern Alaska; oocysts were not detected in moose (A. alces) samples from Alaska nor from muskox (O. moschatus) on Banks Island, Canada ( Johnson et al., 2010; Kutz et al., 2008; Siefker et al., 2002). Prevalence in domestic dogs in the sub-Arctic was low, generally 2–3% (Bryan et al., 2011; Himsworth et al., 2010b; Schurer et al., 2012). In the Yukon Territory, Roach et al., (1993) did not find Cryptosporidium in beaver (C. canadensis), muskrat (Ondatra zibethicus), coyote (Canis latrans), Dall's sheep (Ovis dalli dalli), grizzly bear (Ursus arctos), and wolf (C. lupus) scat. It is possible that Cryptosporidium may not have been detected in early studies because of difficulties in detecting small oocysts on routine faecal flotation. However, even using highly sensitive faecal recovery techniques (sucrose gradient and immunofluorescent antibody specific to Crypto-sporidium), Kutz et al. (2008) did not find Cryptosporidium in muskoxen during the summer of 2004.


Arctic Zoonoses59


Table 2.3 Prevalence [% (n)] of Cryptosporidium in Animals in Alaska and Northern CanadaHost Location Prevalence [% (n)] Method References

Order Artiodactyla

Barren-ground Caribou (Rangifer tarandus groenlandicus)

Teshekpuk Lake and Western Arctic herds, North Slope Borough, AK

6 (49)* IFA Siefker et al. (2002)

Boreal Caribou (Rangifer tarandus caribou)

Trout Lake, Southwestern NT

1.3 (149) SG – IFA Johnson et al. (2010)

Order Carnivora

Dog (Canis lupus familiaris) Bella Bella and Klemtu, BC 3 (35)9 (11)

IFA Bryan et al. (2011)

Mamawetan Churchill River and Keewatin Yatthe, SK

2 (43)2 (66)2 (57)

SG – IFA Schurer et al. (2012)

Northeastern SK 3 (155) SG – IFA Himsworth et al. (2010b)

Order Cetacea

Bowhead Whale (Balaena mysticetus)

Barrow and Kaktovik, AK 5.1 (39) IFA Hughes-Hanks et al. (2005)

North Atlantic Right Whale (Eubalaena glacialis)

Bay of Fundy, NB; Cape Cod, MA

24.5 (49) IFA Hughes-Hanks et al. (2005)



60


Host Location Prevalence [% (n)] Method References

Order Pinnipedia

Ringed Seal (Phoca hispida) Barrow, AK 22.6 (31) IFA Hughes-Hanks et al. (2005)

Nunavik, QC 9 (55)† SG – IFA (intestinal contents)

Dixon et al. (2008)Santin et al. (2005)

Phylum Mollusca

Blue Mussel (Mytilus edulis) Nunavik, QC 72.7 (11) Pooled samples

IFA (tissue) Lévesque et al. (2010)

Within a host species, reports move west to east. Abbreviations for states, provinces, and territories as in Fig. 2.1.IFA – Immunofluorescent assay on faeces unless otherwise indicated, SG – IFA – Sucrose gradient and immunofluorescent assay on faeces unless otherwise indicated.*Caribou-specific genotype.†Observed C. muris and two novel genotypes.

Table 2.3 Prevalence [% (n)] of Cryptosporidium in Animals in Alaska and Northern Canada—cont’d


Arctic Zoonoses 61


In marine mammals, Cryptosporidium spp. have been found in faeces of ringed seals, but not bearded seals, from Alaska (23%) and Nunavik (9%) (Dixon et al., 2008; Hughes-Hanks et al., 2005). On examination of the intestinal contents of ringed seals in the western Arctic region of Canada by immunofluorescence microscopy, Cryptosporidium spp. oocysts were not observed (Olson et al., 1997). Likewise, Cryptosporidium spp. oocysts were not observed in harp or hooded seals from the Gulf of St. Lawrence, Canada (Appelbee et al., 2010). Cryptosporidium spp. were detected in 5.1% of bow-head whales from northern Alaska and 24.5% of North Atlantic right whales from the Bay of Fundy, Canada, and Cape Cod, Massachusetts (Hughes-Hanks et al., 2005). Cryptosporidium was not detected in beluga whales (D. leucas) in Alaska or in the western Canadian Arctic (Hughes-Hanks et al., 2005; Olson et al., 1997).

Viable Cryptosporidium oocysts have been identified in seawater, with the most likely source of contamination being sewage effluent and surface run-off (Appelbee et al., 2005; Robertson, 2007). Migratory Arctic seals may become exposed to Cryptosporidium in sub-Arctic marine environ-ments contaminated with human sewage as well as agricultural run-off.

Figure 2.6 Published reports of Cryptosporidium in animals in the North. (Data from Table 2.3. No human cases have been reported in the published literature).




Experimentally, captive harp seal pups became infected with C. parvum through indirect transmission from the ingestion of seawater contaminated with faeces from experimentally infected seal pups housed in the same tank (Appelbee, 2006). Seals may also become infected through consumption of filter-feeding invertebrates, as Cryptosporidium has been reported worldwide in a variety of bivalve molluscs (Fayer et al., 2004; Robertson, 2007). Cryp-tosporidium was present in 73% of pooled samples of blue mussels collected in Nunavik, Quebec (Lévesque et al., 2010).

The impact of cryptosporidiosis on northern animal populations, espe-cially wildlife, is unknown. Cryptosporidiosis can be clinically significant in young livestock and people, especially if immunocompromised. Apart from disease, other factors may act as stressors adversely affecting the immune system of wildlife and thus rendering them more susceptible to novel infec-tions and their clinical consequences. For example, a heavy infection with Cryptosporidium hominis in a dugong (Dugong dugong) off the east coast of Australia is thought to have contributed to the animal's death (Morgan et al., 2001), probably because it was immunocompromised as a result of another infection or exposure to contaminants from human sewage in the sea-grass beds grazed by the dugong.

4.4. Transmission, Prevalence, and Public Health Impact in the NorthPeople may be infected with a number of species of Cryptosporidium; C. parvum (zoonotic) and C. hominis (human-specific) are the two species most likely to infect people (Appelbee et al., 2005; Graczyk et al., 2008; Thompson et al., 2008). Cryptosporidium is most often transmitted among people by means of direct person-to-person transmission (i.e. the faecal-oral route), or indirectly through oocyst-contaminated drinking water or recre-ational water. Food-borne transmission also occurs but is much less com-mon. In the Arctic, the presence of Cryptosporidium in blue mussels and in the intestinal tract of seals and whales, all of which are food sources for northern residents, should be considered when evaluating the risk to human health.

Since 2000, cryptosporidiosis has been a nationally notifiable commu-nicable disease in Canada, and therefore laboratory surveillance data are available (Fig. 2.7). Based on the limited data available, residents of the three northern territories in Canada may have slightly higher per capita rates of infection with Cryptosporidium than the Canadian average; the pattern is consistent with sporadic outbreak years interspersed with multiple years with few or no reported cases. In Alaska, Cryptosporidium-mean annual


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incidence (1.1 and 0.8 cases/100,000 population) was almost three times less than the U.S. average (2.5 and 2.9 cases/100,000 population) over a two-year time period (2009–2010) (Yoder et al., 2010a), and was consis-tently lower than the U.S. national rate over a 10-year period (Fig. 2.8). Therefore, the evidence suggests that cryptosporidiosis is not currently a significant public health concern under current conditions in the Arctic. Furthermore, the lack of livestock and low level of infection in both marine and terrestrial wildlife indicate that zoonotic transmission of Cryptosporidium may not be common in northern regions. However, access to health care is limited for some northern residents, and this along with challenges in col-lecting and testing faecal specimens may result in a general underdiagnosis of cryptosporidiosis in the North.

There is no effective therapy for cryptosporidiosis in humans or compan-ion animals and maintaining fluid intake is thus essential until the development of immunity results in clearance in immunologically competent individuals

Figure 2.7 Passive surveillance for Cryptosporidium in people in the Yukon Territory (YT), Northwest Territory (NT), Nunavut (NU), and Canada-wide, 2000–2008. [Data from the Noti!able Diseases Online Database of the Public Health Agency of Canada (http://dsol-smed.phac-aspc.gc.ca/dsol-smed/ndis/index-eng.php) and the Canadian Noti!able Disease Surveillance System National Report: 2005–2008].






(Thompson et al., 2008). Although Cryptosporidium infections are usually of short duration and self-limiting in individuals with an intact immune system, the lack of effective anticryptosporidial drugs means the very young, elderly, and immunocompromised may be at risk of severe disease as a result of Cryp-tosporidium infection. An increase in the proportion of northern residents that are immunocompromised, as observed in some regions of northern Canada (Irvine et al., 2011), could lead to an emergence of this disease in the future.

4.5. Future Impact of Climate and Landscape ChangeGiven the similarity of transmission between Giardia and Cryptosporidium, the mechanisms of climate change are likely to be similar for the two para-sites. However, it should be noted that Cryptosporidium does not appear to be as well established at northern latitudes as Giardia, and may therefore have more to gain from a warming, wetter world. In particular, enhanced

Figure 2.8 Passive surveillance for Cryptosporidium in people in Alaska and nation-ally for the United States of America, 1999–2010. (Data from the U.S. Centers for Disease Control summaries of the Morbidity and Mortality Weekly Report Surveillance Summaries, http://www.cdc.gov/healthywater/statistics/surveillance/health_data.html#giardia).



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opportunities for northern agriculture might well lead to introduction of highly suitable domestic livestock reservoirs for zoonotic species of Cryp-tosporidium. From a climate change perspective, it would be interesting to revisit earlier study sites to determine if Cryptosporidium is now present in the environment, animals, and people in the North. If Cryptosporidium is cur-rently excluded from northern regions due to environmental susceptibility of the oocysts, climate change may relax these barriers.

Migratory birds, caribou, and marine mammals could serve as a mecha-nism of introduction into newly susceptible regions. The role of Arctic-nesting geese in transporting pathogens, including Cryptosporidium spp., from sub-Arctic areas should be considered. Canada geese (B. canadensis) are carriers of C. parvum and C. hominis (Graczyk et al., 1998, 2008; Zhou et al., 2004), inhabit freshwater and marine habitats, and migrate throughout northern Canada for summer feeding grounds. Finally, if Cryptosporidium is present at northern latitudes, increased precipitation and frequency of severe weather events could overwhelm existing water treatment infrastruc-ture, with a corresponding increase in the frequency and severity of water-borne outbreaks. Along with Giardia, Cryptosporidium is one of the most common causes of waterborne disease outbreaks in Canada, likely as a result of the resistance of the oocysts to chlorine treatment.

5. TOXOPLASMA GONDII Toxoplasma gondii is a protozoan parasite in the phylum Apicomplexa. Three infective stages of T. gondii exist: tachyzoites, bradyzoites (within tissue cysts), and oocysts. Tachyzoites and bradyzoites result from asexual reproduction and can be produced in both intermediate and definitive hosts, while oocysts are the result of sexual reproduction and are produced in the definitive host (Dubey, 2009). The only known definitive hosts of T. gondii are felids, but numerous intermediate host (IH) species have been described (Frenkel et al., 1970). The primary mechanism for horizon-tal transmission of T. gondii begins when an IH ingests sporulated oocysts from contaminated food, water, or the environment (Fig. 2.9). A secondary mechanism for horizontal transmission occurs via carnivory or cannibalism. Once introduced into a food web, T. gondii can be maintained when one IH ingests tissue cysts from another; this transmission cycle is only perpetuated by asexual reproduction. Vertical transmission occurs transplacentally. If an IH is infected while pregnant, the tachyzoites in the bloodstream will cross the placenta, leading to congenital toxoplasmosis (Dubey, 2009).




5.1. Species and Strains Present in the NorthToxoplasma gondii is the only species in this genus to date. There are three clonal lineages within T. gondii that dominate isolates from domestic ani-mals and people worldwide. Recent characterisation of isolates from North American wildlife has identified a fourth clonal type (Type 12) that domi-nates in wildlife in North America, as well as clonal Type II and atypical genotypes (9, 11) from Alaska. Unspecified atypical genotypes were also reported from Kuujjuaq, Nunavik (Dubey et al., 2010, 2011). Otherwise, little is known about the genotypes of T. gondii present in wildlife, pets, and people in the North.

5.2. Geographic Distribution in the NorthAlmost all reports of toxoplasmosis in animals and people are based on serology, as the organism is rarely detected (Elmore et al., 2012). Antibodies to T. gondii have been reported in animals (Table 2.4) and people (Table 2.5)

Figure 2.9 Life cycle of Toxoplasma gondii in the North. Transmission by oocysts occurs in boreal and sub-Arctic regions where free-ranging de!nitive hosts (felids) are present. Migratory IH (such as Arctic nesting geese, barren-ground caribou, and marine mam-mals) can become infected through consumption of oocysts when they seasonally migrate into terrestrial or marine sub-Arctic environments contaminated with oocysts. Carnivores in arctic regions become infected through consumption of tissue cysts in migratory IH. In all mammalian IH, including felids and people, vertical transmission is likely to occur in females infected during pregnancy.


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Table 2.4 Prevalence [% (n)] of Exposure to Toxoplasma gondii in Animals in Alaska, Northern Canada, and Greenland


Order Anseriformes

Geese Nunavik, QC 4.2 (24) NR Leclair and Doidge (2001)

Order Artiodactyla

Dall’s Sheep (Ovis dalli) Interior Alaska 6.9 (319) MAT Zarnke et al. (2000)Muskoxen(Ovibos moschatus)

Holman, NTKugluktuk, NUCambridge Bay, NU

5 (42)40 (10)5 (151)

MAT Kutz et al. (2000)

Victoria Island, NU 2 (49) MAT Wu et al. (2010)Jameson Land, Greenland 3 (129) Dye test Clausen and Hjort (1986)

Caribou/Reindeer(Rangifer tarandus)

Seward Peninsula, Interior, Southcentral AK 6.6 (241) MAT Zarnke et al. (2000)AK and YT <1 (452) MAT Stieve et al. (2010)Fort Smith, NT 2.9 (104) IHAT Johnson et al. (2010)NT and NU 29.1 (147) MAT Kutz et al. (2001)Leaf River, QC <1 (535) NR Leclair and Doidge (2001)George River, QC/NL 1.2 (82) NR Leclair and Doidge (2001)

Moose (Alces alces) Suscetna R., Alaskan and Kenai Peninsulas 23 (110) IHAT Kocan et al. (1986)North Slope, Interior, Southcentral AK 1.3 (240) MAT Zarnke et al. (2000)

Bison (Bison bison) Interior AK 1 (241) MAT Zarnke et al. (2000)

Continued



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Order Carnivora

Arctic Fox(Vulpes lagopus)

AK (NR) 59.3 (27) DAT Dubey et al. (2011)

Black Bear (Ursus americanus)

Interior Fairbanks and Tanana Flats, AK 15 (40) LAT Chomel et al. (1995)Interior, Southcentral, Southeastern AK 43.4 (143) MAT Zarnke et al. (2000)Alexander Lake, AK 14 (7) MAT Dubey et al. (2010)Kuujjuaq, QC NR Bioassay Dubey et al. (2008)

Dog (Canis lupus familiaris) Fort Resolution, NT 62.5 (56) DAT Salb et al. (2008)Fort Chipewyan, AB 46 (52) DAT Salb et al. (2008)Keewatin-Yatthé, SK 21 (47) DAT, IFA Schurer et al. (2013)

Grizzly Bear (Ursus arctos) AK (multiple sites) 18 (480) LAT Chomel et al. (1995)AK (multiple sites) 25 (892) MAT Zarnke et al. (1997)AK (NR) 66.7 (3) MAT Dubey et al. (2011)

Lynx (Lynx canadensis) Interior AK (multiple sites) 15.3 (255) MAT Zarnke et al. (2001)Polar Bear (Ursus

maritimus)Eastern Greenland 11.1 (108) MAT Oksanen et al. (2009)North Slope, AK; Beaufort and Chukchi Seas 6 (350) LAT Rah et al. (2005)Southern Beaufort Sea, AK 13.2 (136) LAT Kirk et al. (2010)

Red Fox (Vulpes vulpes) AK (NR) 12.5 (8) MAT Stieve et al. (2010)AK (NR) 33.3 (9) MAT Dubey et al. (2011)

Wolf (Canis lupus) AK Interior and Seward Peninsula 17.8 (320) MAT Stieve et al. (2010)North Slope, Interior and Southcentral, AK 8.8 (125) MAT Zarnke et al. (2000)

Wolverine (Gulo gulo) Kugluktuk, NU 41.5 (41) MAT Reichard et al. (2008a)

Table 2.4 Prevalence [% (n)] of Exposure to Toxoplasma gondii in Animals in Alaska, Northern Canada, and Greenland—cont’d



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Order Galliformes

Ptarmigan Nunavik, QC 2.5 (79) NR Leclair and Doidge (2001)

Order Pinnipedia

Pacific Walrus (Odobenus rosmarus)

Southeastern AK to Bering Strait 5.6 (53) MAT Dubey et al. (2003)

Harbour Seal (Phoca vitulina)

Southeastern AK to Bering Strait 16.4 (311) MAT Dubey et al. (2003)NT/NU (multiple sites) 22.2 (9) DAT Simon et al. (2011)

Ringed Seal (Phoca hispida) Tuktoyaktuk, NT 5.9 (17) DAT Simon et al. (2011)Sachs Harbour, NT 7.1 (28) DAT Simon et al. (2011)Ulukhaktok, NT 5.8 (171) DAT Simon et al. (2011)Arviat NU 15.6 (289) DAT Simon et al. (2011)Chesterfield Inlet, NU 2.4 (41) DAT Simon et al. (2011)Hall Beach, NU 23.1 (13) DAT Simon et al. (2011)Sanikiluaq, NU 7.9 (229) DAT Simon et al. (2011)

Bearded Seal (Erignathus barbatus)

NT/NU (multiple sites) 10 (20) DAT Simon et al. (2011)

Seal Nunavik, QC 14 (28) NR Leclair and Doidge (2001)

Reports move from west to east within a host species. Abbreviations for states, provinces, and territories as in Fig. 2.1.NR – not recorded, MAT – Modified agglutination test, IHAT – Indirect haemagglutination test, DAT – Direct agglutination test, LAT – Latex agglutination test, IFA – Indirect fluorescent antibody test.



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Table 2.5 Seroprevalence [% (n)] of Toxoplasma gondii in People in Alaska and Northern Canada

Location Sampling DatesPrevalence [% (n)] Method Reference

Alaska, USA

West, Southeast, Interior 1970–1971 28 (1188) IFA Peterson et al. (1974)16 (1188) IH Peterson et al. (1974)

Canada

Inuvialuit Settlement Region, NT 2007–2008 6 (281) ELISA Egeland et al. (2010a)Keewatin Yatthé Region, SK 2011 14 (201) ELISA Schurer et al. (2013)Nunavik, QC (Multiple sites) 1980s 6 (759) IH Tanner et al. (1987)Nunavik, QC (Kuujjuaq and Salluit) 1983–1986 65 (264) ELISA/IH Curtis et al. (1988)Nunavik, QC (Kuujjuaq) 1987 50 (22) IFA McDonald et al. (1990)Nunavik, QC (Multiple sites) 2004 60 (917) ELISA Messier et al. (2009)James Bay, QC (Multiple sites) 1980s 3 (436) IH Tanner et al. (1987)James Bay, QC (Mistissini) 2005 10 (50) ELISA Lévesque et al. (2007)James Bay, QC (Eastmain and Wemindji) 2007 5 (250) ELISA Campagna et al. (2011)James Bay, QC (Chisasibi and Waskaganish) 2008 9 (266) ELISA Sampasa-Kanyinga et al. (2012)Nunatsiavut, NL (multiple sites) 2007–2008 8 (275) ELISA Egeland et al. (2010b)

Abbreviations for states, provinces, and territories as in Fig. 2.1.IFA – Indirect fluorescent antibody, IH – Indirect haemagglutination, ELISA – Enzyme-linked immunosorbent assay.


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throughout northern Canada and Alaska, and have also been reported in wildlife (muskoxen and polar bears) in eastern Greenland (Fig. 2.10). Anti-bodies have been detected in wildlife as far north as 71°N, and in people at 67°N.

5.3. Transmission, Prevalence, and Animal Health Impact in the NorthIn the North, antibodies to T. gondii have been detected in almost all terres-trial and marine mammals examined, including herbivores and carnivores, as well as some avian species (Table 2.4). The life cycle of T. gondii is unclear in Arctic regions. In boreal and sub-Arctic regions of Alaska and northern Canada, lynx may serve as definitive hosts. Lynx are reported as far North as 68°N in the western Arctic (Reichard et al., 2008a), and 57°N in the east-ern Canadian Arctic (M. Simard, unpubl. obs). In Alaska, 15% of lynx were seropositive (Zarnke et al., 2001), while in southern Quebec, 44% of lynx were reported to carry Toxoplasma antibodies (Labelle et al., 2001); how-ever, efforts to detect oocysts in faeces of lynx have not yet been successful,

Figure 2.10 Published reports of toxoplasmosis in animals and people in Alaska, north-ern Canada, and Greenland, based on immunological methods of detection. (Data from Tables 2.4 and 2.5).




possibly due to the short period of time that oocysts are shed (2–3 weeks in domestic cats), and the difficulty in detecting the small oocysts on routine faecal examination.

Above the tree line in Arctic regions, lynx are not present and domestic felids are uncommon and rarely free-ranging (Miller et al., 2008). There-fore, oocyst transmission is likely restricted to boreal regions in terrestrial ecosystems in the North (Fig. 2.9). Terrestrial Arctic herbivores that sea-sonally migrate into boreal regions (such as barren-ground caribou) and consume oocysts could go on to infect carnivores upon their return to the Arctic. Similarly, arctic nesting geese might introduce the parasite from sub-Arctic and temperate areas into the Arctic, with subsequent transmission to carnivores (Prestrud et al., 2007). Terrestrial carnivores and scavengers (such as Arctic fox, grizzly bears, black bears, dogs, and wolverines) in the North appear to have a higher seroprevalence (generally 10–60%) than her-bivores (generally <10%) (Table 2.4), likely as a result of bioaccumulation through repeated ingestion of infected prey and/or biomagnification up the food chain. Carnivores in coastal regions would also have access to fish and carcasses of marine mammals.

In marine systems, oocysts could be disseminated from sub-Arctic and temperate regions through ocean currents. Oocysts can survive in 4°C in seawater for 2 years and still be infective (Lindsay and Dubey, 2009). Filter-feeding invertebrates and fish may filter and concentrate the oocysts from the marine environment, and remain infective for at least 8 h (Lindsay et al., 2004, 2005; Massie et al., 2010). There is serological evidence that pinnipeds are exposed to T. gondii in the North American Arctic (Dubey et al., 2003; Simon et al., 2011). Most recently, antibodies have been detected in Ant-arctic pinnipeds, suggesting that toxoplasmosis is well established in marine ecosystems worldwide (Rengifo-Herrera et al., 2012).

Toxoplasma gondii may be a concern for the wildlife population health, as the parasite causes abortion and congenital disease in many animal species, including captive reindeer (Dubey et al., 2002). Toxoplasmosis has contrib-uted to mortality in arctic foxes elsewhere in the Arctic (Sorensen et al., 2005). Toxoplasmosis in some wildlife species, such as caribou, may additively influence population declines, triggered by other anthropogenic and envi-ronmental pressures (Kutz et al., 2000; Vors and Boyce, 2009). Barren-ground caribou in the mainland arctic (Bluenose, Bathurst, and Beverly herds, which migrate into the boreal region) are experiencing declines across Canada, and have a relatively high seroprevalence (37% of 117) for antibodies to T. gondii (Kutz et al., 2001), especially for a herbivore (Table 2.4).


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5.4. Transmission, Prevalence, and Public Health Impact in the North5.4.1. TransmissionPeople, like all IH for T. gondii, become infected through consumption of oocysts in contaminated food and water, through consumption of tissue cysts in undercooked fresh meat, and through congenital transmission (Fig. 2.9). The relative significance of these routes of infection in the North is not known. Oocyst transmission is possible wherever domestic cats and lynx are present, largely in sub-Arctic and boreal regions. Although cats are present in Alaskan Eskimo communities (Peterson et al., 1974), domestic cats and lynx are relatively rare in Canadian Inuit populations in Quebec (Messier et al., 2009). Therefore, oocyst transmission is unlikely in Arctic populations, unless ocean currents and watersheds bring oocysts up from sub-Arctic locations. Food-borne transmission in Inuit populations in the North is likely the most significant route of infection with T. gondii, given the important contribution of wildlife to the diet and dietary preferences for raw, fermented, or dried meat. Congenital human transmission has been documented in the Canadian North (McDonald et al., 1990).

5.4.2. PrevalenceIn recent studies, Inuit populations in Nunavik have high seroprevalence (50–65%) for T. gondii (Table 2.5). Seroprevalences were higher in inhabitants from southern and Hudson Bay communities than northern and Ungava Bay communities (Messier et al., 2009). This overall prevalence is 3 times the North American average (23%), and almost double the global average (33%) ( Jones et al., 2001; Tenter et al., 2000). In one Nunavik community, seroprevalence was higher (87%) in the Inuit population than in the sympat-ric Cree population (10%), which was linked to preferences for raw meat in the Inuit population (Messier et al., 2009). In Alaska, however, prevalences between Eskimo (28%) communities on the west coast and on St. Lawrence Island, and Indian communities in interior and southeastern Alaska (30%), were not substantially different (Peterson et al., 1974). Other First Nations and Inuit people living in northern Canada have a relatively low seropreva-lence (5–14% in Table 2.5), which may reflect dietary preferences for cooked meat and consumption of terrestrial (versus marine) wildlife.

5.4.3. Risk FactorsSeroprevalence of T. gondii increased with age in an Alaskan study ( Peterson et al., 1974), and in Canadian Inuit populations in the Inuvialuit (NT) and




Nunatsiavut regions, seroprevalence was higher in people greater than or equal to 40 years-old, as compared to those less than 40 years-old (Egeland et al., 2010a, 2010b). Risk factors for seropositivity for T. gondii in a recent study in Nunavik Inuit (QC) were water consumption, frequent cleaning of water reservoirs, and consumption of seal meat and birds (Messier et al., 2009); seropositive seals, geese, and ptarmigan have been detected in Nun-avik and Nunavut (Leclair and Doidge, 2001; Simon et al., 2011). An epide-miological study of two Cree communities in the James Bay region (QC) showed that seropositivity in this community (which was very low) was associated with being male, hunting, and dog ownership (Campagna et al., 2011). In Alaska, food surveys demonstrated that all community members consumed wild cervids, and about half consumed wild birds, raw eggs of wild birds, and marine mammals, but links to serostatus of individuals were not explored (Feldman, 1974; Peterson et al., 1974).

A food survey administered in the Inuvialuit region found that the food items most commonly eaten in the year prior to the survey were caribou meat (average 67 g/day) and Arctic char (average 116 g/day). Other items consumed were berries, Canada goose, trout, whitefish, beluga oil and cari-bou (heart, ribs, and marrow) (Egeland et al., 2010a). Similarly in Nunatsia-vut, caribou meat (average 67.3 g/day), caribou heart (average 58.5 g/day), and Arctic char (average 52.5 g/day) were the most common items eaten, whereas consumption of berries, rock ptarmigan, Canada goose, partridge, and caribou (ribs and marrow) also contributed to the diet to a lesser extent (Egeland et al., 2010b).

Further investigation is needed into the significance of food-borne routes of transmission of T. gondii in the North, especially the relative con-tribution of migratory caribou, marine mammals, birds, and other wildlife. Determining risk factors at the regional level is a key to implementing cul-turally appropriate and effective local prevention measures, which recognise the importance of wildlife for food security of northern residents.

5.4.4. Impact and ControlToxoplasmosis has been described as the most important parasitic infection in the North American Arctic, in terms of public health impact (Hotez, 2010). Infection with T. gondii has potential to cause human disease, ranging from asymptomatic infections and mild influenza-like illness to severe ocular and neurological lesions, especially in congenitally infected children. The high sero-prevalence in the general population of Nunavik Inuit in Canada led to close monitoring of pregnant women by the regional public health department.


Arctic Zoonoses 75


A survey of 496 women between 1982 and 1987 showed that 4 women in Nunavik seroconverted during pregnancy. Seroconversion was associated with skinning animals for fur and frequent consumption of meat. Seropositive women had eaten between 4 and 8 times more dried seal meat, seal liver, and raw caribou meat than seronegative women (McDonald et al., 1990). From this study, it was determined that congenital transmission led to toxoplasmosis in at least two children. In response, a prevention programme was established in 1996 that requires every pregnant woman in Nunavik to be tested for T. gondii.

Serologic diagnosis is complicated by lifelong persistence of IgG antibod-ies and the potential for prolonged persistence of IgM antibodies ( Montoya and Rosso, 2005). Additionally, the false positive rate of IgM detection can be high, depending on the type of laboratory test performed (Montoya and Rosso, 2005). In response to these challenges, highly specialised tests have been developed to track different antibody levels over time and it is recom-mended that IgM-positive results are confirmed by a Toxoplasma reference laboratory (Montoya and Rosso, 2005).

Control of human T. gondii infections in the North is possible by minimis-ing dietary exposure and potential exposure when handling carcasses, espe-cially during pregnancy. Most recommendations for the control of T. gondii include wearing gloves while handling carcasses, washing hands and kitchen knives frequently when preparing meat, and washing fruits and vegetables before consumption (Kapperud et al., 1996). Additionally, cleaning litterboxes daily, and disposing of litter in a place where it is unlikely to enter the water-shed can minimise the risk of infection from domestic cats. Toxoplasmosis treatment varies by country, but a combination of pyrimethamine, sulfadia-zine, and folinic acid is commonly prescribed (Hotop et al., 2012; Kaye, 2011). Due to potential renal side effects from sulfadiazine therapy, the search for additional treatments is an active field of research (Alvarez et al., 2007).

5.5. Future Impact of Climate and Landscape Change5.5.1. Oocyst TransmissionThere is currently no evidence that oocyst transmission is a significant route of infection in the terrestrial North American Arctic, where felids are not well established. However, as the climate gets warmer, the habi-tat range of lynx and their prey species are predicted to move north-ward with the tree line, facilitating local oocyst transmission. Conditions may also become more permissive for oocyst survival and development. Sporulated oocysts of T. gondii can survive short periods of cold and dehydration, and be infectious for at least 18 months in moist conditions




(Frenkel et al., 1975; Hutchison et al., 1969). An increase in humidity will therefore enhance survival of oocysts, while increased soil temperatures will increase the rate of sporulation of oocysts (Dubey et al., 1970; Lindsay et al., 2002). This increased development rate may trade off with decreased sur-vival of unsporulated oocysts, which experience higher mortality under warmer conditions (Dubey, 2009). If, however, climate change leads to increased winter temperatures, sporulated oocysts may have better survival, as they are susceptible to freezing (Frenkel and Dubey, 1973).

5.5.2. Frequency and Severity of Waterborne OutbreaksWhile oocyst transmission may not be significant under current conditions in terrestrial Arctic ecosystems, oocysts survive in water for long periods, especially in marine systems. Melting of ice and permafrost or landslides, especially along riverbanks, may help transport oocysts to bays and estuaries, where mollusks or other invertebrates can concentrate them, and in turn infect their predators ( Jensen et al., 2010). Increased rainfall and weather extremes will favour the transport and concentration of these oocysts in water systems used by animals and people; indeed, one of the world's largest outbreaks of waterborne toxoplasmosis occurred in western Canada as a result of heavy rainfall washing cougar and cat faeces into a drinking reser-voir (Berkes and Jolly, 2001; Bowie et al., 1997). Water treatment infrastruc-ture in northern communities that does not involve filtration should be considered vulnerable under current and future environmental conditions.

5.5.3. Abundance of and Access to Harvested WildlifeClimate change may alter the habitat available for marine mammals of the Arctic, which may experience loss of ice flows to rest, breed and feed, as well as an increase in weather extremes. Both conditions may result in more animal mortalities (Burek et al., 2008), hence increasing transmission of the parasite to scavengers such as polar bears and arctic foxes, or to invertebrates and marine benthic feeders such as walrus and bearded seals. Loss of near-shore ice platforms may make it more difficult for hunters to harvest marine mammals. If resident hunters (human and wildlife) are forced to switch to more terrestrial diets, they may be exposed to different infection intensities or strains of T. gondii. In addition, new wildlife IH species moving into Arc-tic latitudes from sub-Arctic and temperate systems may bring new strains of T. gondii (Gaydos et al., 2007; Goldstein et al., 2011; Hanni et al., 2003).

There is as yet little evidence for existing effects of climate change on the transmission of T. gondii. Recent increase in the prevalence of exposure


Arctic Zoonoses 77


to T. gondii in polar bears on Svalbard, Norway, was thought to be due to warmer waters in the North Atlantic current, with a corresponding increase in filter-feeding invertebrates and survival of oocysts in marine waters. Other potential changes in infection pressure for T. gondii on Svalbard include an increase of migratory birds as well as increased tourism through cruise ships and other human traffic ( Jensen et al., 2010). In the Canadian Arctic, increased interest in resource exploration in Nunavik and Nunavut has already led to an influx of mining boats and barges, raising concerns about contamination of Arctic waters, and disruption of the migration pat-terns of marine mammals.

6. TRICHINELLA SPP. Nematodes of the genus Trichinella are parasites of carnivores and omnivores in all terrestrial systems and some marine environments globally, and represent the causative agents of trichinellosis among people (Pozio et al., 2009). Species of Trichinella are unique among nematodes in having a “self-contained” (autohexeroxenous) life cycle, where a single vertebrate serves as both DH and IH, harbouring adults and all of the larval stages of the parasite (Fig. 2.11). Transmission is thus dependent on predation or

Figure 2.11 Life cycle of Trichinella species in northern North America L1 = !rst-stage larvae encysted in tissue of host.




scavenging, and typically different species of Trichinella circulate among dif-ferent assemblages of domestic or free-ranging animal hosts (Pozio, 2005).

Adult Trichinella are miniscule (1.0–4.0 mm in length) and live in the small intestine of their hosts, where females produce first-stage larvae that enter the lymphatic system and travel to a variety of sites in the body. Among species of Trichinella circulating amongst placental mammals, larval parasites become encapsulated, whereas those species circulating in avian and other hosts remain free in the muscle tissue, representing life history patterns that are phylogenetically determined (Zarlenga et al., 2006). Only encapsulated forms are known to occur in the North. In the skeletal muscle, the larvae enter the muscle cells as intracellular parasites and become surrounded by a collag-enous capsule. Infection of a new host occurs by predation or by the inges-tion of carrion containing infective larvae. In the intestine of the definitive host, larvae emerge from the capsules, undergo 4 molts, and develop to adult males and females in approximately 3 days (Doyle and Beuchat, 2007; Mit-reva and Jasmer, 2006). Gravid females produce larvae for 3–4 weeks or more until expelled by the host's immune system (Capo, 1996; Dupouy-Camet et al., 2002). First-stage larvae in the musculature are infective by three to four weeks postinfection (Murrell et al., 2000) and can remain infective for years.

6.1. Species and Strains Present in the NorthSpecies of Trichinella include 8 named taxa among 12 distinct genotypes (9 recognised encapsulated and 3 unencapsulated species), all with potential for human infection (Pozio et al., 2009; Zarlenga et al., 2006). During most of the past century, all Trichinella infections were referred to a single species, Trichinella spiralis, thought to circulate widely among domestic omnivores, particularly swine and rats, and a range of wild carnivores, rodents and other mammals. Concepts for broader diversity within the genus were initially developed based on observations about parasite biology and patterns of circulation (Britov and Boev, 1972). These ideas were later corroborated by biochemical and molecular based methods and phylogenetic analyses that define each of the currently recognised lineages (Pozio et al., 2009; Zarlenga et al., 1999, 2006). Consequently, it is now recognised that species of Trichi-nella vary among different regions, and reflect a complex evolutionary and ecological history (Hoberg et al., 2012; Pozio et al., 2009).

Northern latitudes were important in the evolution of the Trichi-nella assemblage following initial origins of encapsulated forms in Eurasia (Hoberg et al., 2012). Diversification in North America (and South America) resulted from independent episodes of geographic expansion and isolation


Arctic Zoonoses 79


with carnivore hosts starting in the late Miocene, nearly 10 million years ago (Pozio et al., 2009; Zarlenga et al., 2006). Events culminating with cli-mate cooling and isolation at high latitudes during the middle Pleistocene (400–500,000 years ago) led to the origins of Trichinella nativa (T-2) and T-6, which remain the primary source of human infections in northern North America today (Hoberg et al., 2012; Pozio et al., 2009; Zarlenga et al., 2006).

Among the 4 species of Trichinella in North America (encapsulated- T. nativa, T-6, T. murrelli; unencapsulated-T. pseudospiralis), only T-6 and T. nativa are known to occur at high latitudes, and only these species have first-stage larvae able to tolerate freezing conditions (Dick and Pozio, 2001). Trichinella nativa is recognised as the primary zoonotic species present in the circumpolar north, whereas Trichinella T-6 is restricted to the North (Gajadhar and Forbes, 2010; Larter et al., 2011; Reichard et al., 2008b). In northern Canada and parts of Alaska, T-6 and T. nativa may occur in sympatry, circulating among an assem-blage of sylvatic hosts including ursids, canids, mustelids, rodents, and marine mammals (Gajadhar and Forbes, 2010; La Rosa et al., 2003; Larter et al., 2011; Pozio et al., 2009; Reichard et al., 2008b). In some regions, hybridisation of T-6 and T. nativa has been observed (La Rosa et al., 2003), and Nunavut and the Northwest Territories in Canada may represent a contact zone between these putative sister-species where populations have come into secondary sym-patry since the termination of the Pleistocene (Dunams-Morel et al., 2012).

6.2. Geographic Distribution in the NorthWildlife and human cases of trichinellosis have been reported in Alaska, northern Canada, and Greenland (Fig. 2.12). In Canada, there are no pub-lished reports on trichinellosis in people in northern British Columbia, Alberta, Manitoba, or Ontario, although Trichinella has been described in wildlife in all provinces and territories in Canada. Reported human cases of trichinellosis generally co-occur with reports of the parasite in free-ranging mammals in the North (Fig. 2.12). Actual geographic limits for northern species of Trichinella have yet to be clearly defined due to the lack of con-temporary surveys, and the fact that most prior records refer to T. spiralis (Rausch et al., 1956). In northern North America trichinellosis has been reported as far north as 78° N in people, and 77° N in animals.

In North America, the predicted range for T. nativa is primarily north of 48° N, associated largely with the tundra to sub-Arctic eco-zones and the 4 °C isotherm (Masuoka et al., 2009). In contrast, T-6 is distributed from the Arctic Circle to temperate regions south of 48° latitude and occurs in zones of sympatry with T. nativa throughout northern Canada and Alaska




(Dunams-Morel et al., 2012; Gajadhar and Forbes, 2010; La Rosa et al., 2003; Larter et al., 2011; Masuoka et al., 2009; Pozio et al., 2009; Reichard et al., 2008b). In northern ecosystems, the distributions of these two encap-sulated species are strongly tied to episodic climate change and exchange of mammals and parasites between Eurasia and North America during the middle to late Pleistocene (Hoberg et al., 2012; Pozio et al., 2009; Zarlenga et al., 2006). Current distributions are to a great extent influenced by host mobility and dispersal; consider the wide-ranging polar bear (Ursus mariti-mus) and arctic fox (Vulpes lagopus) as primary hosts for T. nativa across the Holarctic, and the occurrence of T-6 in large carnivores including bears (U. arctos and U. americanus) and wolverine (G. gulo).

6.3. Transmission, Prevalence, and Animal Health Impact in the North6.3.1. TransmissionFactors influencing the transmission of Trichinella at high latitudes include foraging behaviour and distribution of host species, the structure and function

Figure 2.12 Published reports of trichinellosis in animals and people in Alaska, north-ern Canada, and Greenland. (Data from Tables 2.6–2.9).


Arctic Zoonoses 81


of food chains, and freeze resistance of larvae in tissues of dead mammalian hosts. Species such as polar bears, brown bears, arctic fox, wolves, and wol-verine are highly mobile, disperse rapidly over great distances, and share a broad-based and diverse array of prey species. As opportunistic scavengers, apex predators, and prey for larger carnivores, wolverines may be particu-larly important for transmission of Trichinella (Reichard et al., 2008b; Slough, 2003). In terrestrial systems, other small mustelids (ermine and marten) and arvicoline rodents may also play a role in transmission (Manning, 1960; Rausch et al., 1956). In the North, dogs are often fed on or scavenge meat from harvested carnivores, especially bears and walrus that might be infected with Trichinella. The role of infected dogs in the transmission of the para-site in the North is not known. Other domestic animal hosts for Trichinella (e.g. pigs and horses) are largely absent from northern North America.

In marine systems, transmission of Trichinella among marine mammals has remained somewhat enigmatic. A marine cycle involving polar bears and their primary prey, ringed (P. hispida), bearded (E. barbatus) or harp seals (P. groenlandica) has not been demonstrated, and there are no records of natural Trichinella infections among these phocids from Canada (Forbes, 2000). Trichinella has been found, however, in bearded seals, ringed seals, and an unidentified seal from other sectors of the Arctic (e.g. Russia, Alaska, and Greenland) (Forbes, 2000), but minimal levels of infection suggest that these pinnipeds are peripheral to the primary pathways for transmission in marine systems (Taylor et al., 1985). In the near-shore and pelagic environments associated with pack ice, polar bear and walrus (Odobenus rosmarus) are the most important hosts for Trichinella (Manning, 1960; Taylor et al., 1985).

Walruses are mostly benthic (sea floor) feeders, although some animals actively prey on other pinnipeds (Fay, 1960; Manning, 1960). Diets for wal-rus are dominated by marine mollusks and other benthic invertebrates, although they will opportunistically consume seals and marine birds such as black guillemots (Cepphus grylle), thick billed murres (Uria lomvia), common eider (Somateria mollisima) and arctic fulmars (Fulmarus glacialis) (Fay, 1960; Fay et al., 1990; Gjertz, 1990; Lowry and Fay, 1984; Mallory et al., 2004; Rausch, 1968). It is increasingly recognised that walruses become infected through consumption of freeze-resistant first-stage larvae of T. nativa (or T-6) in carrion (Fig. 2.11). For example, in Greenland, walruses may consume the carcasses of hunted polar bears discarded in the ocean (Kapel, 1997).

Although considered secondary pathways of transmission, Britov (1962) and Fay (1968) showed experimentally that the amphipod crustaceans Gammarus spp., Anonyx nugax, A. laticoxa, and A. affinis that are prey for




some phocids can harbour viable first-stage larvae of Trichinella if fed with infected meat. Additionally, fishes can acquire the larvae following inges-tion of bird droppings or insects that have fed on infected carrion (Hule-back, 1980; Kozlov, 1971); such larvae can remain viable in fish for at least 28 h (Hulebak, 1980). First-stage larvae of T. spiralis remained infective after passing through the intestinal tract of experimentally infected ferrets, polar bears, red foxes, rats, and swine (Smith, 1985; Zimmerman et al., 1959).

There may be extensive overlap between terrestrial and marine cycles of transmission of T. nativa due to natural interactions, such as those observed among brown bears and polar bears feeding on bowhead whale carcasses in Kaktovik, Alaska (Burek et al., 2008), as well as the highly mobile nature of arctic wildlife species, such as polar bears and arctic fox. In addition, human practices, such as leaving carcasses of polar bears out for scavenging, feed-ing polar bear meat to sled dogs, and disposal of dog carcasses on the ice or at sea, may also serve to link terrestrial and marine cycles of transmission (Kapel, 1997).

6.3.2. PrevalenceIn the North, multiple surveys for Trichinella spp. in wildlife have been pub-lished, beginning in 1933 (Masuoka et al., 2009; Polley at al., 2000) (Tables 2.6–2.8). Among northern wildlife, wolverines, polar bears, and brown bears have the highest prevalence of Trichinella spp., whereas black bears (U. americanus), Atlantic walrus (Odobenus rosmarus), and martens (Martes ameri-cana) were reported to have the highest intensity of first-stage larvae in their muscles (means of 117, 99, and 94 larvae per gram, respectively) (Gajadhar and Forbes, 2010). The prevalence of Trichinella in walrus is generally lower than in polar bears but exceeds that observed among phocid seals (Tables 2.6–2.8); intensity of infection in walrus may be relatively high, with a maximum of 1193 larvae per gram of muscle tissue documented (Gajadhar and Forbes, 2010).

Surveys of wildlife in northern Canada have not found Trichinella spp. in Arctic hares (Lepus arcticus), beluga (D. leucas), bearded seal (E. barbatus), harp seal (P. groenlandica), and ringed seal (P. hispida) (see reviews by Appleyard and Gajadhar, 2000; Forbes, 2000; Gajadhar and Forbes, 2010). In sub-Arctic and temperate regions of North America, T. nativa has also been recovered from black bear and cougars (Puma concolor) (Gajadhar and Forbes, 2010), while Trichinella T-6 has been found in brown bear, cougar, and wolverines (Gajadhar and Forbes, 2010; La Rosa et al., 2003; Reichard et al., 2008b; Zimmerman et al., 1959).


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Table 2.6 Prevalence [% (n)] of Trichinella spp. in Animals in AlaskaHost Location(s) Prevalence [% (n)] Method References

Order Carnivora

Arctic Fox (Vulpes lagopus) Adak Island 1 case MD Rausch et al. (1956)Arctic Coast 10 (117) MDSt Lawrence Island 3 (94) MD

Black Bear (Ursus americanus) NR 24 (21) MD Rausch et al. (1956)NR 28 (40) SE Chomel et al. (1998)

Coyote (Canis latrans) Southern AK 13 (8) MD Rausch et al. (1956)Dog (Canis familaris) Adak Island 6 (16) MD Schiller (1952)

Adak Island 7 (13) MD Rausch et al. (1956)Barrow 93 (41) MDSt Lawrence Island 85 (47) MDNR 36 (64) MD

Ermine (Mustela erminea) Brooks Range 43 (40) MD Rausch et al. (1956)Copper River 9 (11) MD Rausch et al. (1956)

Grizzly Bear (Ursus arctos) NR 50 (20) MD Rausch et al. (1956)Multiple sites 49 (878) SE Zarnke et al. (1999)NR 100 (1) TR Pozio (2000)

Least Weasel (Mustela nivalis) Brooks Range 2 cases MD Rausch et al. (1956)Lynx (Lynx canadensis) Brooks Range, Copper River 24 (17) MD Rausch et al. (1956)

Multiple 19 (1065) MD Zarnke et al. (1999)Polar Bear (Ursus maritimus) NR 53 (17) MD Rausch et al. (1956)

NR 47 (478) SE Chomel et al. (1998)Beaufort Sea, Chukchi Sea 56 (500) SE Rah et al. (2005)

Red Fox (Vulpes vulpes) Multiple 41 (76) MD Rausch et al. (1956)Wolf (Canis lupus) Fairbanks 37 (148) MD Zarnke et al. (1999)

Brooks Range 33 (154) MD Rausch et al. (1956)Wolverine (Gulo gulo) NR 50 (38) MD Rausch et al. (1956)

Continued



84


Host Location(s) Prevalence [% (n)] Method References

Order Cetacea

Beluga Whale (Delphinapterus leucas) Wainwright 2 (49) MD Rausch et al. (1956)

Order Lagomorpha

Snowshoe Hare (Lepus americanus) Brooks Range 5 (40) MD Rausch et al. (1956)

Order Pinnipedia

Seals (Various) Arctic Coast, St Lawrence Island <1 (310) MD Rausch et al. (1956)Walrus (Odobenus rosmarus) NR 53 cases NR Fay (1960)

Order Rodentia

Beaver (Castor canadensis) Kalgin Island 3 (29) MD Rausch et al. (1956)Brown Lemming (Lemmus

trimucronatus)Brooks Range 5 (18) MD Rausch et al. (1956)

Brown Rat (Rattus norvegicus) Adak Island, 12 (224) MD Schiller (1952)Multiple sites 11 (261) MD Rausch et al. (1956)

Ground Squirrel (Citellus undulatus) St Lawrence Island <1 (129) MD Rausch et al. (1956)Muskrat (Ondatra zibethicus) Copper River <1 (113) MD Rausch et al. (1956)Narrow-skulled Vole (Microtus gregalis) Brooks Range 2 (57) MD Rausch et al. (1956)Red-backed Vole

(Myodes/Clethrionomys rutilus)Kenai Peninsula 4 (49) MD Rausch et al. (1956)

Red Squirrel (Tamiascurus hudsonicus) Brooks Range, Copper River 4 (94) MD Rausch et al. (1956)

Note that a case is equivalent to a single infected animal.MD – Muscle digest, NR – Not recorded, SE – Serology, TR – Trichinoscopy.

Table 2.6 Prevalence [% (n)] of Trichinella spp. in Animals in Alaska—cont’d


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Table 2.7 Prevalence [% (n)] of Trichinella spp. in Animals in Northern CanadaHost Location(s) Prevalence [% (n)] Method References

Order Carnivora

Arctic Fox (Vulpes lagopus) NT 3 (1566) MD Smith and Snowden (1988)NT 1 case NR Parnell (1934)NU 4 cases BA Chadee and Dick (1982)YT, NU 11 (28) MD Gajadhar and Forbes (2010)

Black Bear (Ursus americanus) Dehcho, NT 6 (120)*,† MD Larter et al. (2011)Wollaston, SK 1 case NR Emson et al. (1972)Black Lake, SK 1 case MD, TR Schellenberg et al. (2003)QC 1 (107) MD Frechette and Rau (1977)NL 1 case MD Butler and Khan (1992)BC, NT, SK, QC 7 (193)*,† MD Gajadhar and Forbes (2010)

Dog (Canis familiaris) Devon Island, NU 1 case TR Kuitunen-Ekbaum (1950)Cape Hopes Advance QC 2 cases TR Kuitunen-Ekbaum (1950)

Grizzly Bear (Ursus arctos) YT 71 (24) MD Choquette et al. (1969)Dehcho, NT 73 (11)*,† MD Larter et al. (2011)BC, NU 29 (68) MD Gajadhar and Forbes (2010)

Lynx (Lynx canadensis) AB 1 case MD Smith and Snowden (1988)BC, NU 7 (107)* MD Gajadhar and Forbes (2010)

Marten (Martes americana) Stony Lake, MB 1 case NR Chadee and Dick (1982)Southern Indian Lake, MB 1 (70) TR Poole et al. (1983)BC, NU 3 (101) MD Gajadhar and Forbes (2010)

Polar Bear (Ursus maritimus) South Beaufort Sea, YT 100 (9) SE Rah et al. (2005)NT 1 case NR Parnell (1934)Cornwallis Island, NU 67 (3) NR Kuitunen-Ekbaum (1950)Southampton Island, NU 67 (3) TR Brown et al. (1949)Churchill, MB 1 case MD, BA Dick and Belosovic (1978)NL 59 (278) TR Thorshaug and Rosted (1956)NU, QC 66 (85)* MD Gajadhar and Forbes (2010)

Continued



86



Red Fox (Vulpes vulpes) NT 11 (19) MD Smith and Snowden (1988)AB 6 (18) MD Smith and Snowden (1988)

Skunk (Mephitis mephitis) AB 6 (124) MD Gajadhar and Forbes (2010)Wolf (Canis lupus) YT 47 (153) MD Choquette et al. (1973)

NT 13 (8) MD Smith and Snowden (1988)NT 47 (153) MD Choquette et al. (1973)Dehcho, NT 52 (27) MD Larter et al. (2011)Fort McMurray, AB 1 case MD Dies (1980)Fort McMurray, AB 1 case NR Smith (1985)AB 33 (3) MD Smith and Snowden (1988)QC 50 (2) MD Smith and Snowden (1988)Nain, NL 1 case BA Smith (1985)NL 4 (48) MD Smith and Snowden (1988)YT, BC, NU 43 (28)* MD Gajadhar and Forbes (2010)

Wolverine (Gulo gulo) Snow Lake, MB 1 case NR Dick (1983)YT, BC, NT 77 (111)*,† MD Gajadhar and Forbes (2010)

Order Pinnipedia

Walrus (Odobenus rosmarus) Southampton Island, NU 4 (394) NR Kuitunen-Ekbaum (1954)Nunavik, QC 12 (52) NR Richardson et al. (2005)NL 10 (74) TR Thorshaug and Rosted (1956)NU, QC 41 (32)* MD Gajadhar and Forbes (2010)

Note that a case is equivalent to a single infected animal. Abbreviations for provinces and territories as in Fig. 2.1.MD – Muscle Digest, NR – Not Recorded, BA – Bioassay, TR – Trichinoscopy, SE – Serology.*T-2.†T-6.

Table 2.7 Prevalence [% (n)] of Trichinella spp. in Animals in Northern Canada—cont’d


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Table 2.8 Prevalence [% (n)] of Trichinella in Animals in GreenlandHost Location(s) Prevalence [% (n)] Method References

Order Carnivora

Arctic Fox (Vulpes lagopus) NR 6 (266) MD Kapel et al. (1995)NR 2 (1591) NR Forbes (2000); Roth and Madsen

(1953)West Greenland 3 (101) MD, TR Rausch et al. (1956); Roth

(1949)Dog (Canis familiaris) NR 62 (945) NR Forbes (2000); Roth and Madsen

(1953)NR 70 (66) MD, TR Rausch et al. (1956); Roth

(1949)NR 67 (227) NR Rausch et al. (1956); Roth

(1950)West Greenland 76 (54) NR Rausch et al. (1956); Thorborg

et al. (1948)Polar Bear (Ursus maritimus) NR 24 (247) NR Forbes (2000); Roth and Madsen

(1953)NR 28 (112) NR Rausch et al. (1956); Roth

(1950)Scoresby Sund 32 (38) MD Born and Henriksen (1990)West Greenland 32 (19) MD, TR Rausch et al. (1956); Roth

(1949)Wolf (Canis lupus) NR 50 (4) NR Forbes (2000); Roth and Madsen

(1953)

Continued



88



Order Pinnipedia

Bearded Seal (Erignathus barbatus)

NR <1 (245) NR Forbes (2000); Madsen (1961)NR <1 (234) NR Forbes (2000); Roth and Madsen

(1953)West Greenland 4 (28) MD, TR Rausch et al. (1956); Roth

(1949)Ringed Seal (Phoca hispida) NR <1 (1775) NR Forbes (2000); Madsen (1961)Seal (Not specified) NR <1 (2318) NR Forbes (2000); Roth and Madsen

(1953)NR <1 (1657) NR Forbes (2000); Madsen (1961)

Walrus (Odobenus rosmarus) NR 1 (489) NR Forbes (2000); Madsen (1961)NR 1 (481) NR Forbes (2000); Roth and Madsen

(1953)Barents Sea,

Greenland Sea15 (47) TR Thorshaug and Rosted (1956)

Thule (Qaanaaq) 4 (24) TR Thing et al. (1976)Thule (Qaanaaq) 2 (126) TR Born et al. (1982)

Note that a case is equivalent to a single infected animal.NR – Not Recorded, MD – Muscle Digest, TR – Trichinoscopy.

Table 2.8 Prevalence [% (n)] of Trichinella in Animals in Greenland—cont’d


Arctic Zoonoses 89


6.3.3. Impact and Control in AnimalsThe clinical significance of Trichinella infection in animals, especially wildlife, is not well known. In Trichinella-naïve grey seals, experimental infections of 5000 to 50,000 larvae resulted in increased sleep, decreased activity, and decreased food consumption. Seventeen days after infection, the seals stopped feeding (Kapel et al., 2003). In temperate regions, Trichi-nella infections (likely T. spiralis) can be clinically significant in domestic dogs and cats, and it seems likely that in the North, T. nativa and T-6 can have similar effects on these hosts, although published reports of infection or disease are few (Desrochers and Curtis, 1987; Fay, 1960). Prevention of trichinellosis in domestic dogs and cats relies on thorough cooking (not freezing) of raw meat prior to feeding and preventing access to human garbage and infected wildlife. Control in sylvatic populations is not logis-tically feasible.

6.4. Transmission, Prevalence, and Public Health Impact in the North6.4.1. Transmission and Risk FactorsSporadic cases and outbreaks of human trichinellosis at high latitudes of North America remain a public health concern. In the North American Arctic, people are currently exposed to trichinellosis through preparation and consumption of raw, undercooked, dried, frozen, or fermented meat from wildlife hosts. Consumption of meat of walrus and bears (polar, grizzly, and black) has caused most of the trichinellosis outbreaks in people across high latitudes of North America (Table 2.9). Caribou, whale, and seal have also been reported to be implicated in some human outbreaks; however, trichinellosis is rare in these species and epidemiological studies including source attribution are not always performed. The size of these animals (bull walrus up to 1200 kg, polar and brown bears up to 550 kg, and black bears up to 270 kg) means that a single carcass can provide meat, and potential exposure to infection, for a large number of people. A few decades ago, Inuit in northern Quebec reported consumption of raw pork products, a potential source of T. spiralis (Ross et al., 1989). However, trichinellosis has been largely eradicated from the Canadian domestic swine herd (Gajadhar et al., 1997) such that all autochthonous cases of trichinellosis in northern Canada are likely of sylvatic origin.

Culturally, patterns and sources of human infection with trichinellosis are directly influenced by food preferences and preparation. Some culi-nary practices appear to have emanated from early recognition of disease



90


Table 2.9 Prevalence [% (n)] and Potential Source(s) of Infection with Trichinella spp. in People in Alaska, Northern Canada, and GreenlandLocation Prevalence [% (n)] Method Source(s) References

Alaska, USA

Anchorage 5 cases CS, SE Black Bear Clark et al. (1972)Barrow 29 cases CS, SE Walrus Margolis et al. (1979)Barrow 4 cases CS Walrus Margolis et al. (1979)Bethel 14 cases CS, SE, EP Black Bear Maynard and Pauls (1962)Goodnews Bay 4 cases CS, SE, EP Brown Bear Maynard and Pauls (1962)AK (NR) 1 case CS, MB Black Bear Wilson (1967)

Canada

Aklavik, NT 15 (87) SE NR Eaton and Meerovitch (1982)Back River, NT 15 (48) ST NR Davies and Cameron (1961)Bathurst, NT 28 (58) ST NR Davies and Cameron (1961)Cape Parry, NT 9 (22) ST NR Davies and Cameron (1961)Fort McPherson, NT 29 (28) SE NR Eaton and Meerovitch (1982)Fort Providence, NT 27 cases NR Black Bear Eaton and Meerovitch (1982)Holman Island, NT 29 (42) ST NR Davies and Cameron (1961)Inuvialuit Region, NT <1 (267) SE NR Egeland et al. (2010a)Inuvik, NT 22 (27) SE NR Eaton and Meerovitch (1982)

22 (250) SE NR Gyorkos and Faubert (1980)Sachs Harbour, NT 2 (101) SE NR Eaton and Meerovitch (1982)Spence Bay, NT 49 (47) ST NR Davies and Cameron (1961)

21 (19) ST NR Davies and Cameron (1961)2 cases CS, MB, ST Polar Bear Davies and Cameron (1961)

Tuktoyaktuk, NT 29 (51) SE NR Eaton and Meerovitch (1982)Black Lake, Stony Rapids, SK 50 cases SE Black Bear Schellenberg et al. (2003)Black Lake, Stony Rapids, SK 40 (78) SE NR Schellenberg et al. (2003)Keewatin Yatthé Region, SK 16 (201) SE NR Schurer et al. (2013)Wollaston Lake, SK 7 cases CS, MB Black Bear Emson et al. (1972)


Arctic Zoonoses91


Arctic Bay, NU 17 (102) SE NR Eaton and Meerovitch (1982)Cambridge Bay (Iqaluktuuttiaq),

NU29 (108) ST NR Davies and Cameron (1961)28 (39) ST NR Davies and Cameron (1961)5 cases CS, SE Grizzly Bear Houzé et al. (2009)

Cape Dorset, NU 95 (20) ST NR Davies and Cameron (1961)33 (9) ST NR Davies and Cameron (1961)95 (20) ST NR Eaton and Meerovitch (1982)

Coral Bay, NU 1 case CS Polar Bear MacLean et al. (1989)Coppermine (Kugluktuk), NU 15 (130) ST NR Davies and Cameron (1961)Eskimo Point (Arviat), NU 1 case CS Whale, Caribou MacLean et al. (1989)Igloolik, NU 30 (100) ST NR Brown et al. (1949)

28 (101) SE NR Brown et al. (1949)King William Land, NU 35 (58) ST NR Davies and Cameron (1961)

18 (11) ST NR Davies and Cameron (1961)Kitikmeot, NU 1 case NR NR Heinzig (1996)Pangnirtung, NU 12 cases CS, MB Polar Bear Emmott and Eaton (1977)Pelly Bay, NU 4 (28) ST NR Davies and Cameron (1961)Pond Inlet, NU 24 cases CS, MB, SE Seal, Whale MacLean et al. (1989)Repulse Bay, NU 16 cases NR NR ProMED, 2003Southampton Island, NU 47 (195) ST NR Brown et al. (1949)

40 (98) SE NR Brown et al. (1949)51 (NR) ST NR Brown (1949)40 (265) SE NR Eaton and Meerovitch (1982)

Eastmain, QC 1 (111) SE NR Campagna et al. (2011)George River, QC 17 cases CS Black Bear Gaulin et al. (2006)Ivujivik, QC 47 cases CS, MB Walrus MacLean et al. (1989)

13 cases CS, MB Walrus, Seal MacLean et al. (1989)Northern QC (NR) 3 (436) SE NR Tanner et al. (1987)

9 (759) SE NR Tanner et al. (1987)Nouveau QC (NR) 5 cases SE NR Laurence et al. (1983)

Continued



92


Nunavik, QC (NR) 8 (36) SE Walrus Proulx et al. (2002)<1 (917) SE NR Messier et al. (2012)

Salluit, QC 32 cases CS, SE Walrus MacLean et al. (1989)13 cases CS Walrus MacLean et al. (1989)62 (68) CS Walrus MacLean et al. (1992)

Wemindji, QC 1 (140) SE NR Campagna et al. (2011)NL, NR 2 cases CS, MB Seal, Bear Coffey and Wigglesworth (1956)

22 (112) SE NR Hockin and Meerovitch (1982)Nunatsiavut Region, NL 1 (275) SE NR Egeland et al. (2010b)

Greenland

Ammasalik (Tasiilaq) 3 (998) SE NR Møller et al. (2010)Attu 6 cases CS, SE Bear, Walrus Møller et al. (2005)Avssakatuk 30 cases CS, SE, ST NR Thorborg et al. (1948)Christianshaab (Qasigiannguit) 12 cases CS, SE, ST NR Thorborg et al. (1948)Claushavn 1 case CS, SE, ST NR Thorborg et al. (1948)Egesdesminde 30 cases CS, SE, ST NR Thorborg et al. (1948)NR 1 (1012) SE NR Møller et al. (2007)

2 cases CS, SE Polar Bear Nozais et al. (1996)Holsteinsborg (Sisimiut) 15 cases CS, SE, ST NR Thorborg et al. (1948)Jakobshavn Kutdligssat (Ilulissat) 32 cases CS, SE, ST Walrus Thorborg et al. (1948)

131 cases CS, SE, ST Walrus Thorborg et al. (1948)Sukkertoppen 2 cases CS, SE, ST NR Thorborg et al. (1948)Kekertak and Ikorfat 37 cases CS, SE, ST NR Thorborg et al. (1948)Thule 1 case NR Walrus Thing et al. (1976)Umanarssuk and Sarkak 5 cases CS, SE, ST NR Thorborg et al. (1948)

Note that a case is equivalent to a single infected person. Abbreviations for states, provinces and territories as in Fig. 2.1.CS – Clinical signs, SE – Serology, EP – Epidemiology, NR – Not recorded, MB – Muscle biopsy, ST – Skin test, T-2 – Trichinella nativa.

Table 2.9 Prevalence [% (n)] and Potential Source(s) of Infection with Trichinella spp. in People in Alaska, Northern Canada, and Greenland—cont’dLocation Prevalence [% (n)] Method Source(s) References


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associated with the consumption of undercooked or improperly prepared meat (Connell, 1949; Rausch, 1951). In northern Quebec, Canada, local customs protective against infection with trichinellosis included thorough cooking of polar bear and arctic fox prior to consumption (Ross et al., 1989). Likewise among the Nunamiut people in the Brooks Range of Alaska, bear was usually only eaten after thorough cooking (Rausch, 1951).

Hunting practices, together with traditional methods of food prepa-ration, remain central to pathways for human exposure and possibly dis-semination of Trichinella. For example, in the Canadian North, walrus are harvested as a communal effort by Inuit using boats. Traditionally, hunts have focused on a limited number of localities where these gre-garious animals gather on pack ice to feed or rest on beaches. Numerous walrus taken during a harvest are killed and butchered immediately and cut into large pieces, either adjacent to or on the boats, or on nearby beaches; some of this meat will be eaten on-site by the hunters. Pieces of the carcasses that cannot be used are usually abandoned on the beaches or floating on the ocean, although some will sink to the ocean floor (M. Simard, personal observations); as carrion these are available to a variety of scavengers. Once the walrus meat is brought into the commu-nities, most is immediately frozen until eaten by people, but some is also fed fresh to dogs. Walrus meat is often eaten frozen, raw, dried (nikku) or fermented (resulting in a product called igunaq). Experimentally, first-stage larvae of T. nativa and T-6 can survive such processing (including freezing) and remain viable for a minimum of 5 months (Forbes et al., 2003).

6.4.2. PrevalenceHistorically, trichinellosis was first reported in people in 1835 (Wood, 1835), and in residents of the Arctic in 1914 (Stefansson, 1914). Fur-ther recognition of cases from different circumpolar countries occurred between 1934 and 1948 through the joint efforts of Stefansson and col-leagues from Europe and North America (Connell, 1949). Records varied from population epidemics in Inuit and Eskimo residents, to European explorers who ate raw polar bears during their expeditions. In Canada, the first documented records were from Southampton Island, Nunavut, where Malcolm Brown from Queen's University discovered in 1948 that 51% of the population responded positively to a skin test for trichinellosis




(Connell, 1949). A few years later, Robert Rausch explored the ecology of Trichinella in marine and terrestrial mammals of Barrow, Alaska (Brandly and Rausch, 1950). In Greenland, an outbreak of trichinellosis in 1947 led to recognition that the parasite was well-established (Thorborg et al., 1948), consistent with a longer historical presence of T. nativa extend-ing into the Pleistocene. Species of Trichinella would have been potential pathogens for the earliest people entering North America across Beringia (Hoberg et al., 2012).

6.4.3. AlaskaAlthough there are many published reports of surveys of Alaskan wildlife for Trichinella (Table 2.6), there are few describing cases in people. Likely the first outbreak reported was in 1944, affected indigenous Alaskans from Yakataga, and was associated with the consumption of insufficiently cooked meat from a local bear (Maynard and Pauls, 1962). A fatal case, again linked to bear meat, occurred in Selawik in 1946 (Maynard and Pauls, 1962), and Rausch et al. (1956) described several outbreaks in the early 1950s affecting both Indigenous and non-Indigenous residents. Subsequently, outbreaks linked to meat from black bear, brown bear, and walrus have been described (Table 2.9). The predominant species of Trichinella in Alaskan wildlife is believed to be T. nativa (T-2), although T-6 and T-2/T-6 hybrids have been detected in Alaskan wolves (La Rosa et al., 2003).

Pooled national surveillance data for 1987–1990, 1991–1996, and 1997–2001 demonstrate that Alaska has been among the four or five states that together experienced many of the cases of trichinellosis in the United States. Annually between 1975 and 2007, the proportion of the U.S. cases that occurred in Alaska ranged from 4% to 70% (Bailey and Schantz, 1990). Historically Alaska has experienced a relatively high incidence rate of this nationally rare disease (total 5 to 65 cases annually in the United States, 1991–2010), likely because of the harvesting and consumption of potentially infected bear and walrus (Adams et al., 2012; Hall-Baker et al., 2010, 2011; Kennedy et al., 2009; Moorhead et al., 1999; Roy et al., 2003). Recently, however, the rate has declined, perhaps in part because of a reduction in the incidence of multicase outbreaks. In Alaska, trichinellosis has been notifiable to the state public health authorities since 1968, and surveillance displays an outbreak pattern of disease with a decline in the size of outbreaks since 2000 (Fig. 2.13).


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No cases of trichinellosis were reported from the state in 12 of the 20 years from 1991 to 2010, and 1992 was the last year in which there were 10 or more cases in a year (Bailey and Schantz, 1990; McAuley at al., 1991; Moorhead et al., 1999; Roy et al., 2003). In addition, risk groups appear to be changing, with recent outbreaks reported in non-Indigenous (versus Indigenous) residents (http://www.epi.alaska.gov/bulletins/docs/ b2000_18.htm).

6.4.4. CanadaIn Canada, trichinellosis was nationally notifiable to public health authori-ties from 1929 until 2000. Surveillance in the Northwest Territories (including the region now known as Nunavut) revealed an outbreak pat-tern of disease with some of the largest outbreaks reported just before the disease was de-listed in 2000 (Fig. 2.14). Approximately three quarters of all reported human cases of trichinellosis in Canada between 1971 and 2000 occurred in the Northwest Territories (including the region now known as Nunavut) and Nunavik, QC (Appleyard and Gajadhar, 2000). Only 3

Figure 2.13 Cases of human trichinellosis reported to the state public health authori-ties in Alaska, 1968–2010.


http://www.epi.alaska.gov/bulletins/docs/b2000_18.htm




human cases have ever been reported in the Yukon Territory, one in each of 1961, 1979, and 1980 (Statistics Canada Annual Report on Notifiable Diseases 1961; Canada Diseases Weekly Report 1980; Canada Communi-cable Disease Report 1994). After 2000, trichinellosis remained notifiable to public health authorities in the Northwest Territories. Since this time, no cases have been reported in the NT, coinciding with the establishment of Nunavut from the eastern portions of what was previously considered the Northwest Territories (http://www.hlthss.gov.nt.ca/english/publications/newsletters/epinorth.asp). Canada-wide, from 2001 to 2005, the risk of hospitalisations (most serious cases) due to trichinellosis was still 2 times higher for residents of Nunavut and Nunavik (incidence = 42/million/year) than for those of the rest of Canada (incidence = 0.09/million/year)(Gilbert et al., 2010).

Despite sporadic cases and outbreaks, recent surveys in Canadian Inuit in communities from Nunatsiavut, Nunavik (QC), and the Inuvialuit (NT)

Figure 2.14 Cases of human trichinellosis in the northwest territories (including the eastern portion now known as Nunavut) between 1961 and 1999, as reported to national public health authorities in Canada. In 1999, 37 cases were from Nunavut, with the other 4 from the northwest territories. The disease was de-listed for surveillance in 2000.


http://www.hlthss.gov.nt.ca/english/publications/newsletters/epinorth.asp

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settlement regions report low seroprevalences (less than 1%) ( Egeland et al., 2010a, 2010b; Messier et al., 2012). Seroprevalence results from recent stud-ies in Cree communities in Northern Quebec are also low, between 0 and 1% (Campagna et al., 2011; Lévesque et al., 2007; Sampasa-Kanyinga et al., 2012). However, in a Dene population from northern Saskatchewan in the sub-Arctic region of Canada, trichinellosis seroprevalence was high (16%), (Schurer et al., 2013), suggesting that transmission is ongoing (Table 2.9).

6.4.5. GreenlandThe first reported outbreak of what was believed to be trichinellosis in people in Greenland occurred in 1933 near Nugssuak, and the likely source of infection was walrus. A second outbreak in 1944 in Holsteins-borg, with walrus the probable source, included 63 cases, and 20 deaths. Subsequently, in 1947, there were outbreaks in several communities total-ling 295 cases and 33 deaths (Thorborg et al., 1948) (Table 2.9). Between 1949 and 1959, more than 100 additional cases were reported (Møller et al., 2005), but none between 1959 and 1971 (Møller et al., 2010). This may in part reflect a lack of detection; in communities with out-breaks, some people were likely infected without clinical signs and in the absence of an outbreak, individual clinical cases might not have been recognised. Since 1971, only 9 cases have been reported in the published literature (Table 2.9).

Currently in Greenland, as elsewhere, diagnosis of trichinellosis in people is most often based on a patient's history, especially risk factors for infection, clinical signs (including haematology and blood chemistry), and serology using an enzyme-linked immunosorbent assay (ELISA), sometimes supplemented by a Western blot (Møller et al., 2005). In recent studies, the incidence of trichinellosis in Greenland has decreased and seroprevalence has been low (1–3%) (Møller et al., 2005, 2007, 2010). This likely reflects societal shifts from traditional foods and food preparation techniques to a more western diet, coupled with greater awareness of the disease (Pars et al., 2001). Also, since 1966, inspection of all polar bear and walrus meat has been mandatory in Greenland, but this is not always enforced or performed by trained personnel (Møller et al., 2010).

To date, T. nativa (T-2) is the only species found in Greenland (La Rosa and Pozio, 1990), and consumption of raw or undercooked meat from polar bears and walrus remains the major source of human infection. A recent survey of 1012 children aged 8–14 years from several




communities in Greenland demonstrated a seroprevalence of 1.1% for Trichinella (Møller et al., 2007). In a second multicommunity survey of 998 people aged 10 years or older, seroprevalence increased with age, from 1.4% in people aged 40 years or younger to 12.3% in peo-ple aged 60 years or older. Overall, significant risk factors for infec-tion were ‘occupation as hunter or fisherman’ and ‘intake of polar bear meat’ (Møller et al., 2010). While almost all reported cases have been in Greenland residents, in 1994, two visitors from France acquired clini-cally apparent infections from polar bear meat they consumed while in Greenland (Nozais et al., 1996).

Assuming that the prevalence of Trichinella in a wide range of Greenland wildlife observed in early surveys has been maintained (Table 2.8), con-sumption of meat from free-ranging animals, especially polar bears and wal-rus, will remain a risk for people in Greenland. This risk could be to some extent mitigated by increased education, and by standardised preconsump-tion testing of high-risk species, as practised for walrus in some northern communities in Canada (Proulx et al., 2002). Hunting and the consumption of wildlife in Greenland, however, are likely to remain an important part of the cultural fabric of the Kalaallit, as they are for many northern residents. Opportunities to continue these traditions, with minimal risk of disease, should be protected.

6.4.6. Impact and Control in PeopleHealthcare personnel in the North must maintain an index of suspicion of clinical trichinellosis, which can present as a vague myalgia, in order to pursue a detailed food history and to order appropriate laboratory testing. Symptoms associated with infection with T. nativa have been decribed as primary and secondary trichinosis, caused by differences in humoral responses (MacLean et al., 1992). The primary syndrome asso-ciated with larvae in the muscle is characterised by oedema, fever, rash, and myalgia. The secondary syndrome, mostly reported in previously infected individuals with acquired immunity, is associated with persistent diarrhoea, and few of the syndromes observed in primary trichinosis. These differences are thought to be linked with timing and intensity of IgG and IgM antibody response. Trichinellosis is suspected when a patient shows one or more clinical signs coupled with high eosinophil counts and an epidemiological investigation implicating consumption of potentially infected meat as a risk factor (Proulx et al., 2002). Blood


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can be sent to a hospital laboratory to confirm the diagnosis with an ELISA (MacLean et al., 1992; Serhir et al., 2001). When the suspected meat source is still available for testing, the double separatory funnel and digestion technique can be used to confirm the presence of the parasite (Proulx et al., 2002). Once the potential source of infection has been established, and there is a risk that other people in the community may be infected, a health advisory is broadcast, warning of the risks, sources of infection, and prevention measures (cooking or discarding the meat). Treatments sometimes tried are anthelmintic drugs (i.e. mebendazole or albendazole), and steroids (i.e. prednisone) for serious cases, depending on the clinical signs (Kennedy et al., 2009; Møller et al., 2005; Proulx et al., 2002; Schellenberg et al., 2003).

In recent years in some regions of northern Canada, there is increased awareness of and local diagnostic capacity for trichinellosis. In Nunavik, Quebec, a programme was initiated in 1992 to use a double separa-tory funnel and digestion technique to test walrus tongues for Trichi-nella infection prior to consumption, and to have the results available to hunters within 24 h (Leclair et al., 2003). The Nunavik Trichinellosis Prevention Program (NTPP) is based at the Nunavik Research Center in Kuujjuaq. If a walrus is found to be infected, it is recommended that the carcass is destroyed or the meat is eaten only after it is well cooked. It is also recommended that meat from an uncooked infected carcass is not to be fed to dogs.

An interesting consequence of the NTPP is that hunters in Nunavik sometimes avoid the area from which an infected walrus has been har-vested, perhaps for several years, and hunt further from their community. This unfortunately decreases the yearly harvest since it costs more to pay for fuel to reach more distant hunting areas. Another consequence of the NTPP is that hunters harvest younger animals, which are better tasting and less likely to be heavily infected with Trichinella. As a consequence of the NTPP, there have been no cases of trichinellosis due to walrus harvested in Nunavik since 2000, although one person from Nunavik was infected from untested walrus meat eaten at a community feast in Nunavut (Larrat et al., 2012). A testing programme has been in place in Nunavut since 2003. The Northwest Territories has been using the same techniques to monitor T. nativa and T-6 in terrestrial carnivores. Despite the development and expansion of programmes for diagnosis of




Trichinella, it takes time for people to learn and adjust to the screening programme (Larrat et al., 2012).

Trichinellosis may be declining in people in many areas of the circumpolar North, in part due to control programmes such as that implemented in Nunavik, as well as shifts in diet to store-bought foods and changes in storage and preparation methods for meat from wild-life. However, while people younger than 40 years of age eat more store-bought food, many northern residents (86% of people from Inu-vialuit, NT, and 25% from Nunatsiavut in Northern Labrador) still prefer to eat ‘country foods’ (Egeland et al., 2010a, 2010b). In Nun-avik, people still consume 8.7 meals/week of country food (Blanchet and Rochette, 2008). Active hunters are present in 57%, 25%, and 45% of the households studied in Inuvialuit, Nunatsiavut, and Nunavik, respectively (Blanchet and Rochette, 2008; Egeland et al., 2010a, 2010b). Harvesting capacities have diminished over time due to lack of money for transportation, gas and supplies, scarcity of animals, bad weather, and lack of time. Fortunately, those that continue to hunt still share their food, an important cultural activity and a source of high quality nutrition in communities facing chronic food inse-curity (lack of available, affordable, culturally acceptable, safe and high-quality food). For example, 26–50% of women in northern Canada could not afford to buy food at the store (Lambden et al., 2006). Finally, successful public health messages emphasise the importance of traditional foods that provide physical and social well-being, cultural identity, economic value, and food security (Blanchet and Rochette, 2008; Egeland et al., 2010a, 2010b). Tools such as the Canadian food guide now include country foods for Inuit and First Nations peoples (http://www.hc-sc.gc.ca/fn-an/food-guide-aliment/index-eng.php, http://rrsss17.gouv.qc.ca/index.php?option=com.contentandview=article&id=215&Itemid=138&lang=en). Finally, recognition of new risk groups (visitors and new northern residents) has led to develop-ment of targeted public health information, such as that provided to the out-of-state bear hunters in Alaska (http://www.adfg.alaska.gov/index.cfm?adfg=blackbearhunting.blackbrown).

6.5. Future Impact of Climate and Landscape ChangeThere is no current evidence that prevalence or intensity of Trichinella has responded to climate or environmental change; however, there has been limited surveillance and adequate comparative baselines are generally


http://www.hc-sc.gc.ca/fn-an/food-guide-aliment/index-eng.php

http://rrsss17.gouv.qc.ca/index.php%3foption%3dcom.contentandview%3darticle%26id%3d215%26Itemid%3d138%26lang%3den

http://rrsss17.gouv.qc.ca/index.php%3foption%3dcom.contentandview%3darticle%26id%3d215%26Itemid%3d138%26lang%3den

http://www.adfg.alaska.gov/index.cfm%3fadfg%3dblackbearhunting.blackbrown

http://www.adfg.alaska.gov/index.cfm%3fadfg%3dblackbearhunting.blackbrown

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not available. Accelerated warming is likely to have the most important effects on the ecology of Trichinella through changes in the behaviour, diet, and distribution of mammalian hosts. Warming will lead to modified migration routes for terrestrial and marine mammals through responses to changing patterns of snow cover, extent of sea ice and other envi-ronmental variables. For example, in the Hudson Bay area of Canada, changes in the mean timing of ice freeze-up and break-up of 0.8–1.6 weeks have already been observed (Hochleim et al., 2010). These changes in turn will influence the availability, quality, and species composition of forage species in terrestrial and marine systems. For example, polar bears, walrus, and ringed seals rely on ice platforms, and disruption of sea ice can alter the location, extent and duration of these formations leading to interference with resting, feeding, and breeding for these marine mam-mals. Extreme events associated with climate change could also cause hypothermia, drowning, or stranding from exhaustion among wildlife (Burek et al., 2008).

New migration routes associated with habitat availability for mam-mals may further influence shifts in foraging behaviour and diet, through alterations in species composition, density, and distribution of pelagic fishes and invertebrates as primary prey (Rausch et al., 2007). Among pagophilic (ice-associated) marine mammals, such shifts in nearshore food webs are predicted to directly influence the structure and diversity of parasite faunas (Rausch et al., 2007). For example, over the past decade, the edge of the permanent and annual pack ice has moved further off-shore and considerably beyond the 100 m contour that defines the limit of diving depth for Pacific walrus. As a consequence, walrus are now occupying habitats beyond the typical foraging range, and diets are shift-ing from mollusks and benthic invertebrates to other marine mammals and carrion.

Concurrently, there are increasing opportunities for overlap among marine and terrestrial cycles of transmission of trichinellosis. Increasing numbers of polar bears from the Beaufort Sea, northern Alaska, and the Chuckchi Sea are remaining on the land in summer and early fall. This is leading to more encounters with brown bears because both are scavenging bowhead whales that strand at that time of year (Burek et al., 2008). Similarly, an increase in carcasses on islands and ice packs can also increase interac-tions among marine mammals (walruses, seals) and bears (polar and brown). This new abundance of carrion and prey has the potential to increase Trichi-nella transmission among walrus, polar bears, and seals, and to modify the




distribution of species of Trichinella, and influence the potential for human infection (Rausch et al., 2007).

First-stage larvae of Arctic-adapted species (T. nativa and T-6) in car-casses are uniquely adapted to survive freezing conditions (Dick and Pozio, 2001). The degree of tolerance depends on several factors that might be affected by climate change, including absolute temperature, number of freeze-thaw cycles, host species, and duration of infection (Davidson et al., 2008; Gottstein et al., 2009; Kapel et al., 1999, 2003). Shifting isotherms may determine new contact zones for T. nativa and T-6 relative to T. mur-relli, which is typically distributed at temperate-boreal latitudes. Addition-ally, species now distributed in the southern region of North America, including T. spiralis and T. murelli, may also be introduced into higher lati-tudes as environments become increasingly permissive for agriculture and new zones of contact are established for species of Trichinella circulating in sylvatic and domestic cycles.

Finally, changes in human behaviour may alter the risks of transmission of Trichinella in a warming North. Indigenous residents of the North may be at decreasing risk of exposure due to increased awareness, capacity for local detection, and changing food preferences and preparation techniques. However, enhanced access to the North American Arctic (i.e. through increased number of ice-free days in the Northwest Passage) may increase the numbers of visitors, many of whom lack protective traditional knowl-edge and therefore may be at increased risk of trichinellosis. For exam-ple, recent emergence of cruise boat tourism in the Canadian North has included many passengers who want to sample regional foods. In addition, foreign hunters who come to the North to experience living in the tundra and hunting their own food may be at risk of infection (Ancelle et al., 2005; Gaulin et al., 2006; Houzé et al., 2009; Nozais et al., 1996).

7. TOXOCARA SPP. Ascarid nematodes are members of the Order Ascaridida, of which the Family Toxocaridae are the focus of this review. Life cycles of these ascarids are often direct. Adult nematodes inhabit the GIT of the vertebrate host. Unembryonated eggs are passed in faeces of the DH and larvae develop in the eggs at rates dependent on abiotic conditions. New definitive hosts become infected upon ingestion of eggs containing second-stage larvae. For Toxocara spp., larvae undergo complex migration routes depending on age and immune status of the host, and transplacental


Arctic Zoonoses 103


and/or transmammary infection may occur within definitive hosts. The life cycle of Toxocara may also involve vertebrate paratenic hosts (PHs) with second-stage larvae encysting in tissue and infecting DHs upon ingestion (Fig. 2.15). For Toxascaris leonina, the life cycle may be direct or indirect, with second-stage larvae developing to third-stage larvae in the tissue of an IH, and definitive hosts become infected through con-sumption of the IH. Vertical transmission is not thought to occur for this species.

7.1. Species Present in the NorthToxocara canis and Toxocara cati, zoonotic nematodes responsible for ocular and visceral larval migrans in people, are present in sub-Arctic regions of northern Canada and Alaska (Fig. 2.16). Their presence is not well docu-mented in Arctic regions of North America, and neither species has been reported in Greenland. Other ascarid nematodes reported in carnivores in the North include Toxascaris leonina and Baylisascaris spp. other than B. pro-cyonis; however, the zoonotic potential of these parasites is considered low (Choquette et al., 1969, 1973; Eaton and Secord, 1979; Gau et al., 1999; Rausch and Fay, 2011). Toxascaris leonina has been identified as a potential cause of eosinophilia in people in Alaska (Rausch and Fay, 2011).

Figure 2.15 Life cycle of the canine roundworm, Toxocara canis. The infective stages for people are second-stage larvae (L2) in eggs or in tissues of PHs (L1 – !rst-stage larvae).




7.2. Geographic Distribution in the NorthToxocara eggs have limited survival in cold climates and are not regularly reported in wild or domestic carnivores in Arctic regions of North America (Fig. 2.16, Table 2.10). In Canada, the northernmost reports of T. canis origi-nated from dogs (Canis lupus familiaris) in Cape Wolstenholme, QC and Fort Rae, NT (both 63° latitude), while the northernmost report of T. cati originated from lynx in northern Alberta (54° latitude) (Cameron et al., 1940; Unruh et al., 1973; van Zyll de Jong, 1966). In Alaska, Toxocara spp. have been reported in lynx (L. canadensis; presumably T. cati), as well as dogs and wolves (C. lupus; presumably T. canis) (Dau, 1981). Laboratory evidence indicates that T. cati eggs survive in colder conditions than T. canis (O’Lorcain, 1995), suggesting that T. cati may have a more northern distri-bution; however, case reports are sparse from the northern distribution of either parasite. Eggs/adults of T. leonina have been reported as far north as 73° latitude, suggesting that efforts based on faecal surveillance could have detected eggs of T. canis, which are morphologically distinct from those of Toxascaris and Baylisascaris (Choquette et al., 1973).

Figure 2.16 Published reports of adults or eggs of Toxocara canis in dogs in the North (data from Table 2.10) and seropositive people (data from Table 2.11). No clinical cases of larval migrans have been reported in the North.


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7.3. Transmission, Prevalence, and Animal Health Impact in the NorthToxocara canis transmits predominantly among canids (dogs, wolves, coy-otes, and foxes), through a variety of routes, including transplacental, transmammary and faecal-oral; however, small mammals also play a lim-ited role as PHs (Fig. 2.15). In the last century, dogs and wild canids at latitudes greater than or equal to 58°N in the North were not commonly infected with T. canis. In dogs, the parasite was not detected in 272 fae-cal samples from dogs in northern Alberta, nor in 80 faecal samples or 14 intestinal tracts from dogs in Kuujjuaq, QC (Desrochers and Curtis, 1987; Unruh et al., 1973). In wild canids, postmortem examination of 173 wolves (C. lupus) from 60 to 80° latitude in the Yukon, Northwest Territories, and Ellesmere Island, Nunavut, Canada failed to identify T. canis, as did necropsy of 50 Arctic fox (V. lagopus) from Banks Island, NT (73°N) (Choquette et al., 1973; Eaton and Secord, 1979). A recent study in two communities at 59 and 61°N in western Canada found the prevalence of T. canis in dogs to be 3 and 7%, respectively (Table 2.10) (Salb et al., 2008), suggesting that this parasite may be more successful at Arctic latitudes in recent times.

Table 2.10 Prevalence [% (n)] of Toxocara canis in Dogs (Canis lupus familaris) in Alaska and Northern Canada

Location LatitudePrevalence [% (n)] Methods References

Alaska, USA

NR NR <1 (414) N Rausch and Fay (2011)Adak 51°N 31 (16) N Schiller (1952)

Canada

Fort Rae, NT 63°N <1 (1000) F Unruh et al. (1973)Fort Resolution, NT 61°N 7 (70) F Salb et al. (2008)Fort Chipewyan, AB 59°N 3 (59) F Salb et al. (2008)13 locations, SK 50–57°N 30 (3370) F Allen and Mills (1971)Loon Lake, La

Ronge, SK54–55°N 48 (160) F Unruh et al. (1973)

1 location, SK !53°N 17 (155) F Himsworth et al. (2010b)

3 locations, SK 55–59°N 11 (167) F Schurer et al. (2012)Moosonee, ON 51°N NR N Cameron et al. (1940)Wolstenholme, QC 63°N NR N Cameron et al. (1940)

Abbreviations for states, provinces and territories as in Fig. 2.1.NR – Not recorded, N – necropsy, F – faecal flotation or sedimentation.




Prevalence of T. canis was higher in dogs at latitudes less than 58°N (as opposed to north of this latitude) in Alaska and Canada, ranging from 30 to 48% in the last century, with lower prevalence (11–17%) in two recent studies in western Canada (Table 2.10) (Allen and Mills, 1971; Himsworth et al., 2010b; Schiller, 1952; Schurer et al., 2012; Unruh et al., 1973). This may reflect changes in dog demographics (more pets as compared to sled dogs) and better dog management practices. In wild canids from temper-ate regions of Canada, T. canis has been reported in wolves from Manitoba (1/601; 0.2%) and Alberta (2/98; 2%); coyotes (C. latrans) from Newfound-land (13/69; 19%) and Alberta (1/75; 1%); and red fox (Vulpes vulpes) from New Brunswick and Nova Scotia (43/61; 71%) (Baron, 1970; Holmes and Podesta, 1968; Smith, 1978; Stronen et al., 2011).

Horizontal and vertical transmissions of T. cati occur among felids, as well as via predator–prey interactions between felid DHs and rodent PHs. While transplacental infection is the primary route of transmission for canids, felids are most commonly infected by transmammary routes, and secondarily by ingestion of encysted larvae and embryonated eggs (Overgaauw and van Knapen, 2008). In northern Alberta, the prevalence of T. cati was 3.5% in 133 lynx examined by necropsy, as opposed to 22% in 274 lynx trapped in various boreal regions of northern Ontario (Smith et al., 1986; van Zyll de Jong, 1966). The prevalence of this parasite in other felid species, including domestic cats, is currently unknown in the North.

Toxocara spp. do not generally cause severe adverse reactions in defini-tive hosts, and it is unlikely that the health of northern canids and felids is significantly compromised. However, high-infection intensities in transpla-centally infected puppies can result in a pot-bellied appearance, failure to thrive, and, although rare, intestinal blockage and/or death. Juveniles are more likely to be infected than adults and are more likely to exhibit clini-cal symptoms (Roddie et al., 2008; Smith et al., 1986). Companion animals can be effectively treated by anthelmintic administration; however, veteri-nary services and prescription drugs are generally inaccessible in the North (Brook et al., 2010; Jenkins et al., 2011).

Rodents infected by T. canis may exhibit a variety of behavioural and cognitive changes that impair survival and fitness relative to the intensity of infection (Cox and Holland, 2001). These changes might increase vulnera-bility to predation by canids and felids, ultimately completing the nematode life cycle. Human hosts are known to experience adverse effects associated with migrating larvae (pain, vision impairment, seizures), but it is unclear whether animals are similarly affected. Postmortem examination of rats


Arctic Zoonoses 107


(Rattus norvegicus) experimentally infected by T. cati revealed L2-stage larvae in a variety of tissues including the muscle, eye, liver, kidney, brain, and lung (Santos et al., 2009).

Treatment and control of ascarids focuses on anthelmintic administra-tion for definitive hosts (such as domestic dogs and cats), and on maintain-ing high standards of hygiene with regard to pet faeces. Treatment of PHs is unusual. A wide variety of commercial products are available to treat Toxocara spp. in the definitive host. Formulations generally include one or more of the following: pyrantel, piperazine, nictroscanate, and milbemycin to target adult worms; and emodepside, ivermectin, moxidectin, selamectin, and fenbendazole to treat both adult worms and larvae (Ramsey, 2011). Fenbendazole, moxidectin, and the avermectins are used to prevent vertical transmission of Toxocara in pregnant and lactating females. The Canadian Parasitology Expert Panel recommends treating dogs with an anthelmintic effective against roundworms at 2, 4, 6, and 8 weeks of age, followed by a monthly regimen until 6 months of age, and then followed by annual, bi-annual, or tri-annual treatment depending on the individual animal's risk factors for exposure. The recommendation for cats is identical except that kittens begin treatment at 3, 5, 7, and 9 weeks of age (Beck et al., 2009).

7.4. Transmission, Prevalence, and Public Health Impact in the NorthPeople become infected with larvae of Toxocara spp. through accidental ingestion of embryonated eggs shed by definitive hosts, or through con-sumption of uncooked meat from PHs (Fig. 2.15). Eggs shed by canids and felids are not immediately infective for people or animals, and require a period of maturation in the environment. Theoretically, people could come into contact with embryonated eggs of Toxocara adhered to the peri-anal region of cats and dogs (Overgaauw et al., 2009; Roddie et al., 2008). How-ever, a number of studies focused on risk factor assessment have demon-strated that pet ownership is, in fact, protective against exposure to T. canis (Iddawela et al., 2003; Schantz et al., 1980; Won et al., 2008; Yang et al., 1982). The prevalence of Toxocara spp. in people is directly proportional to the rates of soil contamination with infective eggs of Toxocara, demonstrat-ing that ingestion of eggs in a contaminated environment is the most com-mon route of infection for people (Mizgajska, 2001).

Clinical disease associated with Toxocara spp. is characterised by visceral or ocular larval migrans; however, some individuals remain asymptomatic (‘covert toxocariasis’). In Canada, human cases are rare, and are most likely




to occur in children and those experiencing pica (Fanning et al., 1981; Schantz et al., 1980). Larval migrans due to Toxocara spp. have not been reported in people in the Canadian North, Alaska, or Greenland. In the USA, there appears to be a southern bias, with 57% of 44 recent cases of ocular toxocariasis occurring in residents of the southern U.S. states (http://www.cdc.gov/mmwr/preview/mmwrhtml/mm6022a2.htm). Recent seroprevalence studies in Canada conducted between 2004 and 2012 demonstrate that exposure is low (<1–4%) in residents of NT, NL, and QC (Table 2.11). In a recent study in Nunavik, QC, residents of the Hudson Bay region were 3.5 times more likely to be seropositive than those in the more northern Ungava Bay region (Messier et al., 2012). This is a logical finding given the known sensitivity of Toxocara eggs to freez-ing temperatures and the low prevalence of T. canis in wildlife and dogs at Arctic latitudes.

Table 2.11 Seroprevalence [% (n)] of Toxocara canis for People Residing in Northern Canada

Location LatitudeSampling Dates

Prevalence [% (n)] References

Inuvialuit Settle-ment Region, NT

68–72°N 2007–2008 <1 (362) Egeland et al. (2010a)

Keewatin Yatthé Health Region, SK

55–59°N 2011 13 (201) Schurer et al. (2013)

Nunavik, QC (Multiple sites)

55–62°N 1980s 11 (759) Tanner et al. (1987)

Nunavik, QC (Multiple sites)

55–62°N 2004 4 (917) Messier et al. (2012)

James Bay, QC (Multiple sites)

48–53°N 1980s 10 (436) Tanner et al. (1987)

James Bay, QC (Mistissini)

50°N 2005 4 (48) Lévesque et al. (2007)

James Bay, QC (Eastmain and Wemindji)

52°N and 53°N

2007 3 (250) Campagna et al. (2011)

James Bay, QC (Chisasibi and Waskaganish)

54°N and 51°N

2008 4 (266) Sampasa-Kanyinga et al. (2012)

Nunatsiavut, NL (Multiple sites)

54–56°N, 58–62°W

2007–2008 1 (310) Egeland et al. (2010b)

Abbreviations for states, provinces and territories as in Fig. 2.1.


http://www.cdc.gov/mmwr/preview/mmwrhtml/mm6022a2.htm

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Diagnosis of human toxocariasis is based on ocular examination and/or serology. It is important to note that serological tests for T. canis can cross-react with other helmiths, such as T. leonina, which is the dominant ascarid in domestic and wild canids at Arctic latitudes (Nicholas et al., 1984; Park et al., 2002; Rausch and Fay, 2011). Cross-reactions may account for higher seroprevalence (10–11%) reported in older studies with less-specific tests (e.g. Tanner et al., 1987 in Table 2.11). In addition, there are other parasitic causes of ocular larval migrans (such as larvae of Baylisascaris and some trematode species), which may account for a recent finding that 30% of 20 patients clinically diagnosed with ocular toxocariasis in the USA in 2009–2010 were seronegative on ELISA for antibody to Toxocara spp. (http://www.cdc.gov/mmwr/preview/mmwrhtml/mm6022a2.htm).

Treatment of toxocariasis in people differs according to the severity of symptoms and the location of second-stage larvae. Patients with visceral larval migrans are administered anti-parasiticides (such as albendazole, thia-bendazole, and mebendazole), and may also be given anti-inflammatory corticosteroids to relieve symptoms caused by severe allergic response. Cases of ocular larval migrans are generally treated with corticosteroids, and may also require ophthalmologic procedures (Despommier, 2003).

7.5. Future Impact of Climate and Landscape ChangeToxocara spp. nematodes may pose a greater risk of exposure for other DHs, PHs, and people in the North if environmental conditions become more suitable for eggs to survive and embryonate. In general, eggs require two to six weeks at temperatures between 10 and 30 °C before the eggs reach an infective stage, with accelerated development at warmer temperatures. Therefore, warming temperatures in the North may lead to accelerated embryonation in the environment. This may be offset by the fact that eggs of T. canis do not embryonate in darkness (Feney-Rodriguez et al., 1988), suggesting a relatively inflexible seasonal window of opportunity for eggs to embryonate at northern latitudes.

In addition to influencing rate of embryonation, temperature is an important limiting factor for survival of eggs of Toxocara, with both devel-opment rates and viability decreasing with increasing time at freezing tem-peratures; eggs of T. cati may be more freeze tolerant than those of T. canis (Azam et al., 2012; O’Lorcain, 1995). At the other end of the spectrum, eggs do not survive at temperatures above 37–40 °C for long (Gamboa, 2005); however, in northern regions of North America, the lower temperature threshold is likely the most important. The proposed lower temperature


http://www.cdc.gov/mmwr/preview/mmwrhtml/mm6022a2.htm



threshold for survival of eggs of T. canis is approximately "15° C (Gillespie, 1988). Embryonated eggs can survive on the soil surface and/or beneath snow cover, even at air temperatures reaching "26 to "29° C (Azam et al., 2012; Ghadrian et al., 1976; Levine, 1968). Toxocara eggs are also sensitive to arid conditions and desiccate quickly in direct sunlight (Mizgajska, 2001). Therefore, warmer and wetter conditions in the North will likely favour enhanced survival of eggs of Toxocara, especially in winter.

Scavenging of PHs may be an important route of transmission of Toxo-cara spp., especially in sylvatic cycles. Second-stage larvae encysted in the muscle tissue of dead PHs are sensitive to variations in temperature and humidity. Larvae of T. cati encysted in the muscle tissue can survive refrig-erator temperatures (!4° C) for two weeks and remain infective for mice; however, the larvae lose motility and viability after three weeks in a refrig-erator and 12 h in a household freezer ("25° C) (Taira et al., 2012). Larvae encysted in tissues of PHs for at least two to three weeks have increased survival at freezing temperatures as compared to larvae in newly infected PHs (Sprent, 1953). Therefore, freeze tolerance and age of infection may be important factors for transmission through scavenging of PHs in adverse northern conditions, as well as food safety aspects for northern residents, if food preparation methods fail to inactivate encysted larvae.

The present geographic distribution of Toxocara rarely exceeds 60° lati-tude in North America and the parasite is apparently absent in Greenland. However, T. canis has recently been identified in northern dog popula-tions where it was absent 35 years previously (Jenkins et al., 2011; Salb et al., 2008; Unruh et al., 1973). This is likely due to the movement of southern companion animals into northern communities, coupled with warming temperatures that allow Toxocara eggs to embryonate and to sur-vive for longer periods of time in the environment. In addition, as vertical routes of transmission exist for both T. cati (transmammary) and T. canis (transplacental), female pets brought into the North could create pock-ets of infection, even under currently unfavourable climatic conditions. Resource extraction opportunities and climate change may continue to drive an influx of people and pets from temperate regions into the North, where lack of veterinary services and canine overpopulation might facili-tate human exposure to zoonotic species of Toxocara.

In addition to domestic dogs, wild canids may also be moving north. Arctic fox in Canada are not currently reported as hosts for T. canis, but in southern areas of the country, the prevalence of infection in red fox popula-tions has been high (71–95%) (Baron, 1970; Eaton and Secord, 1979; Smith,


Arctic Zoonoses 111


1978). Climate change has resulted in the expansion of red fox north-wards into what was previously arctic fox territory and the establishment of sympatric arctic and red fox populations (Hersteinsson and Macdonald, 1992). Thus, natural range expansion of wildlife hosts could contribute to establishment of T. canis in Arctic regions of North America, and possibly Greenland, leading to a spillover into local wildlife. Previously uninfected definitive host populations (e.g. wolves, arctic fox) shed eggs at higher rates than previously exposed hosts, and given the right climatic conditions, an environment can quickly become contaminated with eggs of Toxocara (Overgaauw and van Knapen, 2008; Roddie et al., 2008). Adult female T. canis nematodes can shed millions of eggs per day into the environment, depending on infection intensity and host immune status (Glickman and Schantz, 1981).

To summarise, climate change may drive the range expansion of Toxo-cara spp. into Arctic areas where they are not currently well established. In sub-Arctic regions of North America where Toxocara spp. are already established, climate warming could lead to amplification of transmission due to enhanced survival of eggs in the environment and larvae encysted in muscles of dead PHs during winter, more rapid embryonation of eggs in the environment during summer, and higher levels of egg shedding by previ-ously uninfected hosts.

8. ANISAKID NEMATODES Anisakid nematodes are members of the Family Anisakidae, which includes several zoonotic genera. Anisakids are present in aquatic environ-ments worldwide, infecting invertebrates, fish, birds, and marine mammals. The whaleworm (Anisakis simplex) and sealworm (Pseudoterranova decipiens) are the most common zoonotic parasites in marine systems. Anisakis simplex uses cetaceans as definitive hosts, whereas P. decipiens prefers seal species as definitive hosts (Klimpel et al., 2004; Palm, 1999).

Within the definitive host, adult nematodes are present in the digestive system, and the female nematodes release eggs into the marine environ-ment through the faeces of the host (Fig. 2.17). Depending on the species, eggs embryonate and larvae undergo two or three moults before hatching, releasing second or third-stage larvae in the marine environment (Hays et al., 1998; Køie et al., 1995). Copepods serving as PHs or IHs (depending on species of anisakid nematode) ingest the larvae. In turn, copepods can be eaten by larger invertebrates (such as isopods, amphipods, polychaetes,




and mysids), fish, or cephalopods serving as PH. Larger pelagic and demersal fish may act as PH by eating smaller benthic fish. In PH, third-stage larvae migrate through the digestive system, and invade organs and flesh, where they encapsulate (Anderson, 2000). The life cycle is completed when the definitive hosts, such as marine mammals, eat infected PH (fish or inverte-brates).

8.1. Geographic Distribution in the NorthAnisakid nematodes have been detected in wildlife, predominantly marine mammals, seabirds, and marine and anadromous fish, across northern North America as far north as 70°N (Fig. 2.18; Table 2.12).

8.2. Species and Strains Present in the NorthSpecies of Anisakis, Pseudoterranova (syn. Phocanema, Porrocaecum, Terranova), Contracaecum, Phocascaris, and Hysterothylacium have been identified in the

Figure 2.17 Simpli!ed, generic life cycle of anisakid nematodes such as Anisakis simplex (whaleworm) and Pseudoterranova decipiens (sealworm). De!nitive and paratenic hosts (PH) can become infected by consumption of intermediate (IH) or PH at any point in the life cycle. People are considered dead-end or accidental hosts, in which third-stage larvae (L3) generally do not develop.


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North and Greenland (Table 2.12). In the 1990s, enzyme electrophoresis research discovered genetically distinct siblings within species of Anisaki-dae. For example, the A. simplex species complex is now recognised as containing A. simplex C, A. pegreffii, A. physeteris and A. simplex sensu stricto (Mattiucci et al., 1997).

In the North, a biogeographical model estimates that A. simplex (s. str.) is present in the waters of the North Atlantic, Greenland, and up the Pacific Coast to the Aleutian Islands of Alaska (Kuhn et al., 2011). The only other Anisakis species present in the North is A. simplex C, located along the coast of British Columbia (Mattiucci et al., 1997). In the North Atlantic, P. decipiens A, B, and C are present in the marine food chain (Paggi et al., 1991, 2000), whereas Contracaecum osculatum A, B, and C are present in Arc-tic and boreal marine species (Mouritsen et al., 2010; Nascetti et al., 1993). C. osculatum B and C have been described in grey seals (Halichoerus grypus), and C. osculatum B in harbour seal (P. vitulina), harp seal (P. groenlandica), and hooded seal (C. cristata) (Mattiucci and Nascetti, 2008). The develop-ment and application of PCR techniques have led to the characterisation

Figure 2.18 Published reports of anisakid nematodes in animals and people in Alaska, northern Canada, and Greenland. (Animal data from Table 2.12).



114


Table 2.12 Prevalence [% (n)] of Anisakid Nematodes (Family Anisakidae) in De!nitive Avian and Mammalian Hosts, and Fish PH, in northern North America

Host Location(s)Prevalence[% (n)] Parasite Identi!cation References

Class Aves, Order Charadriiformes

Common Murre (Uria aalge) Northwest Atlantic <1 (667) Anisakis sp. Muzaffar (2009)<1 (667) Contracaecum spp.3 (667) C. spiculigerum

Thick billed Murre (Uria lomvia) Northwest Atlantic 6 (119) C. spiculigerum Muzaffar (2009)

Class Mammalia, Order Cetacea

Beluga Whale (Delphinapterus leucas) Mackenzie Delta, NT 20 (10) A. simplex Wazura et al. (1986)100 (10) C. aduncum

Nunavik, QC 79 (19) Anisakidae spp. Pufall et al. (2012)Churchill, NU 1 case A. simplex Doan and Douglas

(1953)Blue Whale (Balaenoptera musculus) Arctic and North

Pacific OceansAt least 7

casesA. simplex, Anisakis sp.,

Pseudoterranova decipiensMeasures (1993)

Bowhead Whale (Balaena mysticetus) Barrow, AK 1 case Anisakis sp. Migaki et al. (1982)

Class Mammalia, Order Pinnipedia

Bearded Seal (Erignathus barbatus) Arviat, NU; Nain, NL 75 (16) Anisakidae spp. Pufall et al. (2012)Fur Seal (Callorhinus ursinus) St-Paul Island, AK 2 (250) Anisakis spp. Spraker et al. (2003)

35 (250) Contracaecum spp.92 (250) Pseudoterranova spp.

Harbour Seal (Phoca vitulina) Glacier Bay and Prince William, AK

85 (84) Anisakis spp. Herreman et al. (2011)8 (84) Contracaecum spp.

6 (84) P. decipiensRinged Seal (Phoca hispida) QC, NU, NL 18 (170) Anisakidae spp. Pufall et al. (2012)Spotted Seal (Phoca largha) Bering Sea, AK 71 (55) C. osculatum Shults (1982)

25 (55) P. decipiens


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Class Osteichthyes

Arctic Char (Salvelinus alpinus) Nunavik, QC 18 (22) Anisakidae spp. Pufall et al. (2012)Ungava Bay, QC 32 (62) Contracaecum spp. Desdevises et al. (1998)Multiple, NL 9 (35) Anisakis sp. Hicks and Threlfall

(1973)3 (35) Contracaecum spp.3 (35) C. aduncum

Multiple, Greenland 3 (348) A. simplex Due and Curtis (1995)1 (348) Contracaecum spp.

2 (348) C. osculatum/C. phocae1 (348) Hysterothylacium aduncum<1 (348) P. decipiens

Atlantic Cod (Gadus morhua) Ungava Bay, QC 44 (313) Anisakis sp. Curtis (1984)41 (313) Contracaecum or Phocascaris

West Greenland 24 (227) Anisakis sp. Mouritsen et al. (2010)74 (227) C. osculatum

1 (227) H. aduncumAtlantic Salmon (Salmo salar) Nunavik, QC 8 (36) Anisakidae spp. Pufall et al. (2012)

Multiple, NL 53 (71) Anisakis sp. Hicks and Threlfall (1973)3 (71) C. aduncum

Atlantic Tomcod (Microgadus tomcod) Nain, NL 64 (25) Anisakidae spp. Pufall et al. (2012)Atlantic Whitefish (Coregonus huntsmani) Nunavik, QC 8 (26) Anisakidae spp. Pufall et al. (2012)Brook Trout (Salvelinus fontinalis) Multiple, NL 4 (124) Anisakis sp. Hicks and Threlfall

(1973)1 (124) Contracaecum sp.Chum salmon (Onchorhynchus keta) Cordova, Nushagak, AK 100 (40) A. simplex Karl et al. (2011)Fish, multiple species* Aleutians and SE AK 60 (124) Anisakis sp. Moles and Heintz

(2007)10 (124) Contracaecum spp.27 (124) H. aduncum15 (124) P. decipiens



116


Greenland Cod (Gadus ogac) West Greenland 8 (64) A. simplex Mouritsen et al. (2010)84 (64) C. osculatum

Greenland Halibut (Reinhardtius hippoglossoides)

NL, Davis Strait, Greenland

10†, 43‡ (609) A. simplex Boje et al. (1997)45† (609) Contracaecum spp.5† (609) H. aduncum1†, 2‡ (609) P. decipiens

Lake Trout (Salvelinus namaycush) Multiple, NL 3 (31) C. aduncum Hicks and Threlfall (1973)

Pink Salmon (O. gorbuscha) Cordova, AK 100 (12) A. simplex Karl et al. (2011)Polar Cod (Boreogadus saida) Nunavik, QC 69 (51) Anisakidae spp. Pufall et al. (2012)Sable Fish (Anoplopoma fimbria) Sitka, AK 100 (25) Anisakidae spp. Heckmann and Otto

(1985)Sculpin, Longhorn (Myoxocephalus

octodecemspinosus)Nunavik, QC 86 (14) Anisakidae spp. Pufall et al. (2012)

Sculpin, Shorthorn (M. scorpius) Nunavik, QC 50 (26) Anisakidae spp. Pufall et al. (2012)Sockeye Salmon (O. nerka) Puget Sound, AK 100 (NR) A. simplex Deardorff and Kent

(1989)Cordova, Nushagak,

Naknek, AK100 (50) A. simplex Karl et al. (2011)

Abbreviations for states, provinces, and territories as in Fig. 2.1.NR – Not recorded.*Pacific sand lance (Ammodytes hexapterus), Pacific herring (Clupea pallasii), Pacific cod (Gadus macrocephalus), Dusky rockfish (Sebastes ciliatus), Pacific smelt (Tha-leichthys pacificus), Alaska pollock (Theragra chalcogramma), Rock sole (Lepidopsetta bilineata), Capelin (Mallotus villosus), Arrowtooth flounder (Atherestes stomias), Atka mackerel (Pleurogrammus monopterygius).†Prevalence based on detection of larvae in alimentary tract.‡Prevalence based on detection of larvae in fillets and/or body cavity.

Table 2.12 Prevalence [% (n)] of Anisakid Nematodes (Family Anisakidae) in De!nitive Avian and Mammalian Hosts, and Fish PH, in northern North America—cont’d

Host Location(s)Prevalence[% (n)] Parasite Identi!cation References


Arctic Zoonoses 117


of Anisakis spp., Contracaecum spp., Hysterothylacium aduncum, and Porrocaecum spp. in marine and freshwater fish, marine mammals and fish-eating birds in the Circumpolar North from the Okhotsk, Bering and Norwegian Seas (Kijewska et al., 2002).

8.3. Transmission, Prevalence, and Animal Health Impact in the NorthAnisakid nematodes were first reported in the North American Arctic as early as 1899 (Stiles and Hassall, 1899). Anisakid nematodes have been docu-mented in a wide range of definitive hosts, primarily marine mammals and birds, and fish PHs in the North American Arctic and Greenland (Table 2.12). Anisakis sp. has also been reported in other mammals, such as sea otters (Rausch et al., 2007) and a brown bear (U. arctos) in Alaska (Davey, 1971). Reports of anisakid species from the Arctic generally stem from studies to evaluate the potential impact on commercial fisheries (Boje et al., 1997; Curtis, 1984; Deardorff and Kent, 1989; Desdevises et al., 1998; Heckmann and Otto, 1985; Hicks and Threlfall, 1973; Karl et al., 2011; Moles and Heintz, 2007), or are incidental reports during necropsy of stranded marine mammals (Doan and Douglas, 1953; Measures, 1993; Migaki et al., 1982). As well, Arctic bird studies have included helminth fauna as indicators of climate change (Hoberg, 1996; Muzaffar, 2009). In the Eastern Canadian Arctic, zoonotic anisakid species are present in marine fish species (such as Atlantic tomcod, polar cod, and sculpins) and definitive hosts (such as ringed seals, bearded seals, and beluga) that are consumed by Inuit (Pufall et al., 2012). In the western Arctic (Alaska), salmon are important PHs (Table 2.12) and larvae of A. simplex have been reported at low prevalence (<1%) in krill IH (Euphausia pacifica and Thysanoessa raschii) in Prince Wil-liam Sound, Alaska (Smith and Snyder, 2005).

Fauna and prevalence of anisakids in animals varies by region, as well as age, sex, and dietary preferences of the host. For example, ringed seals in two Inuit communities in the Hudson Bay region of Canada harbour different species of anisakid nematodes, probably due to differences in diet (M. Simard, unpublished data). Prevalence and abundance of anisakid nema-todes in seals differed significantly depending on Arctic or Atlantic waters in different Norwegian fjords, diet of seals, and fish age class (Johansen et al., 2010). Adult male seals were more heavily infected than females or juveniles. In fish, anadromous fish are less likely to be infected than estuarine fish (Pufall et al., 2012). Prevalence of A. simplex in Atlantic and Greenland cod increases with age, and peaks at age class 2 to 4 when the diet switches




from crustaceans (infected with one or two larvae) to capelin, that may har-bour many anisakid larvae (Mouritsen et al., 2010). This shift has also been demonstrated in Atlantic cod from the western Atlantic (McClelland, 2002).

Species of Anisakidae can show marked differences in regional abundance and host specificity. Terranova decipiens (now P. decipiens) were most abundant in Icelandic and Plateau cod, but almost absent in fisheries from Greenland, Faroe Bank, and the Arctic sea of Norway (Platt, 1975). In contrast, Anisakis sp. were present in all fisheries stock from all regions, with prevalence more variable in North Atlantic cod (10–83%) than in cod from Arcto-Norwegian waters (95%). In general, A. simplex has low definitive host specificity com-pared to other Anisakidae (Klimpel et al., 2004). Anisakid nematodes also differ in their IH preferences, with A. simplex detected in large, deep sea, crustacean IHs (Copepoda and Euphausiacea), H. aduncum in planktonic and benthic invertebrates, and Pseudoterranova in benthic Crustacea (Klimpel and Rückert, 2005; Klimpel et al., 2006; Køie, 1993).

Anisakid nematodes can cause pathology in both definitive and paratenic animal hosts, but the overall impact on health and fitness has not been well described. In marine mammals, the majority of anisakid nematodes are in the stomach: the fundic region in seals, and the anterior region in cetaceans. Larvae or adults can be attached alone, or they may be found in clusters. Pathology is variable and includes local granulomatous inflam-matory responses, gastric nodules, and/or gastric ulcerations. Inflammation (macrophages, leukocytes, and giant cells) may also be present as deep as the muscularis externa (Bishop, 1979; Fleischman and Squire, 1970; McClelland, 1980; Migaki et al., 1971, 1982; Smith and Wootten, 1975; Spraker et al., 2003; Wilson and Stockdale, 1970; Young and Lowe, 1969). Intestinal perfo-ration associated with anisakid nematodes contributed to mortality in many sea otters in Alaska (Rausch et al., 2007). There is one report of Contracaecum sp. in the brain of a striped dolphin (Martin et al., 1970).

In fish PHs, depending on the parasite and fish species, anisakid larvae can be recovered on organs, in the flesh, or both. Postmortem migration of Anisakis sp. larvae from organs to flesh has been observed in herring (Clupea harengus) (Smith, 1984; Smith and Wootten, 1975), although this was not observed in salmon in Alaska (Karl et al., 2011). In Norway and England, A. simplex is the cause of red vent syndrome in Atlantic salmon, where inflam-mation and haemorrhage occurs around the vent. In severe cases, erosion of the skin, scale loss, and moderate to severe haemorrhage may occur. The cause of this syndrome is still unknown, but it does not seem to affect the general body condition of the animal (Beck et al., 2008; Noguera et al.,


Arctic Zoonoses 119


2009). There are documented cases in Northern Quebec, Canada, raising concerns that the parasite may be emerging (M. Simard, unpubl. data).

8.4. Transmission, Prevalence, and Public Health Impact in the NorthPeople are infected by anisakid nematodes through consumption of raw, smoked, marinated, salted or undercooked fish or invertebrates. Ingested larvae are thought to remain at the third stage (although see Ishikura et al., 1995; Lichtenfels and Brancato, 1976), and people are generally considered accidental or dead-end hosts (Fig. 2.17). Third-stage larvae of A. simplex and P. decipiens are the most common causes of the disease called anisaki-dosis (or anisakiasis), present in people worldwide. Other species such as A. physeteris, A. pegreffii, Contracaecum spp. and Thynnascaris spp. can also cause the disease (Audicana and Kennedy, 2008; Hochberg and Hamer, 2010; Ishikura et al., 1990).

The passage of larvae in the oesophagus may create a tingling sensation in the throat, and larvae may be coughed out or vomited. If the parasite is retained, it can attach to the stomach or intestinal mucosa (Audicana and Kennedy, 2008). Diagnosis can be confirmed by visualisation of nematodes on endoscopy, followed by removal and morphological identification of nematodes. A week after invasion of the anisakid nematode, patients may experience nausea, vomiting, diarrhoea, abdominal pain, and hypersensi-tivity reactions. Symptoms may last for several weeks to 2 years. In rare cases, anaphylactic shock is possible. Allergic reactions have been reported by consumption of infected cooked or raw fish and anchovies in vinegar. Fishermen and workers in fish processing plants can become sensitive to this nematode (Audicana and Kennedy, 2008).

Despite relatively high prevalence in fish consumed by people in the North (in 102 Alaskan salmon examined, prevalence of infection with A. simplex was 100% – Karl et al., 2011), human cases appear to be relatively uncommon. As many cases may be asymptomatic or only mildly symp-tomatic, it is likely that cases are underdiagnosed, and there is no formal surveillance or reporting structure for human cases of anisakidosis. Clinical cases have been reported in Alaska, including reports of human infections with Pseudoterranova (Desowitz, 1986; Gyorkos et al., 2003; Lichtenfels and Brancato, 1976; Myers, 1970). In one case, a fourth-stage larva was removed from the throat of a patient (Lichtenfels and Brancato, 1976). Ten percent of stools studied in Eskimos from the Bethel area were infected with imma-ture larvae identified as Anisakis sp. and Porrocaecum (syn. Pseudoterranova)




sp. (Hitchcock, 1950). Outbreaks in Alaska have been associated with con-sumption of undercooked salmon (6 people in Chitina), as well as raw halibut (2 people in Glenallen) (http://www.epi.alaska.gov/bulletins/docs/b1982_24.htm; http://www.epi.alaska.gov/bulletins/docs/b1987_19.htm).

The only report of anisakidosis in Arctic Canada is in an Inuk woman in Nunavik, QC, who had eaten raw Arctic char (Bhat and Clelland, 2010). This person was referred to a southern specialist after complaining of epi-gastric pain, weight loss, and fatigue to the local nursing station (Bhat and Clelland, 2010). Her symptoms resolved upon endoscopic removal of a single third-stage larva of Anisakis sp. Elsewhere in Canada, one case of Ani-sakis sp. due to consumption of raw Pacific Salmon and a case of P. decipiens in a person in Nova Scotia have been reported (Couture et al., 2003; Kates et al., 1973). No clinical cases of anisakidosis have been reported in Green-land. In the only serosurveillance study specific for anisakidosis in the Arctic, Møller et al. (2007) reported a seroprevalence of 0.9% in 1012 children from Greenland. These results were considered an underestimation due to the short life of IgG antibodies.

8.5. Future Impact of Climate and Landscape ChangeAnisakid species will react differently to climate change according to the environmental tolerance of free-living stages and changes in fish host populations. Eggs and newly hatched larvae are particularly dependent on the temperature, pH, salinity, oxygen, and turbidity of their marine envi-ronment (Rokicki, 2009). Therefore, enhanced coastal water melting and freshwater run-off will alter the development of these stages. Water tem-perature and salinity demonstrably influence egg hatching of P. decipiens. Experimental laboratory research shows that larvae hatch faster in warmer waters (5 °C–15 °C), and survive longer in brackish and salt waters com-pared to freshwater (Measures, 1996). At "17 °C, development of eggs of Contracaecum rudolphii is inhibited (Dzieko"ska-Rynko and Rokicki, 2007).

Declines of Anisakis sp. off the coast of Labrador coincided with different climatic conditions and absence of capelin (Mallotus villosus) and cod (Gadus morhua) in the coastal Labrador waters (Khan and Chandra, 2006). Decrease in prevalence of P. decipiens and corresponding increase in prevalence of C. osculatum in Atlantic cod, other groundfish and grey seals from the Gulf of St Lawrence between 1988 and 1992 is believed to be due to warmer water temperatures stemming from the Labrador current. This favoured C. osculatum (in which eggs can hatch at 0 °C) as compared to cold-adapted P. decipiens (Marcogliese, 2001). Therefore, climate change could lead to





Arctic Zoonoses 121


faunal shifts in anisakid nematodes. Furthermore, warmer water will favour the northward migration of pelagic fish, and this may expand the range of anisakids in the North and amplify endemic transmission of Anisakis sp. (Marcogliese, 2001; Perry et al., 2005; Rokicki, 2009).

Final hosts such as marine mammals, especially those that are pagophilic (dependent on floating ice), will be affected by warmer waters. It is pre-dicted that feeding habits and diet will change due to reduction of available ice habitat for resting, feeding, and breeding; changes in migration pat-terns; and loss of substrate for prey (Burek et al., 2008; Rausch et al., 2007). Changes in host migratory patterns can result in marked changes in sea-sonal abundance of anisakid nematodes; for example, northward migration of whales and a spring plankton bloom resulted in a peak in abundance of A. simplex in saithe (Pollachius virens), cod (G. morhua), and redfish (Sebastes marinus) in Norway coastal waters (Strømnes and Andersen, 2000).

From the perspective of Arctic residents, some of whom consume dried marine mammal intestines and raw fish, amplified endemic transmission and faunal shifts in anisakid nematodes to more temperate-adapted species would likely result in altered risk of human exposure to zoonotic species. Detection of the magnitude and direction of these changes will require enhanced monitoring of prevalence in people and animals, as well as spe-cies-level identification of larvae in fish to determine zoonotic potential.

9. DIPHYLLOBOTHRIID CESTODES Diphyllobothriids (the broad fish tapeworm and relatives) are well-recognised zoonotic parasites, with an estimated 20 million people infected throughout the world (Chai et al., 2005). Typical representatives of the order Diphyllobothriidea (formerly Pseudophyllidea; see Kuchta et al., 2008) are characteristic cestode parasites in piscivorous birds and mammals, and collec-tively have widespread distributions globally in freshwater and marine envi-ronments (Deliamure et al., 1985; Dick, 2008; Scholz et al., 2009). These are among the largest cestodes in the world, with adults in some species attaining up to 15–25 m in length, in excess of 4000 segments, and with infections that may persist for over 20 years (Scholz et al., 2009). Evidence of a long association with people is indicated by documentation of diphyllobothriosis among coastal populations in Peru extending to 4500 years ago (Reinhard and Urban, 2003). In North America, diphyllobothriids have been associated with people since the earliest incursions out of Eurasia (Hoberg et al., 2012; Rausch and Hilliard, 1970; Rausch et al., 1967; Scholz et al., 2009).




Among these cestodes, faunal structure has been determined by both nat-ural events of expansion and isolation over the Quaternary (2.6 million years ago) and more recent anthropogenic drivers for introductions and establish-ment that may extend to the late Pleistocene linking Eurasia and North America. Translocation and introduction during the last century have also been significant mechanisms for establishment of species of Diphyllobothrium in freshwater habitats (Adams and Rausch, 1997). Diphyllobothriids have been associated with people coincidental with the earliest incursions out of Eurasia into North America and in conjunction with diets rich in both freshwater and anadromous fishes that serve as IHs and PHs (Hoberg et al., 2012; Rausch and Hilliard, 1970; Rausch et al., 1967; Scholz et al., 2009). These cycles are likely the sources for infection of early immigrants into North America prior to European exploration and contact, and would have driven circulation of cestodes coincidental with marine and aquatic fisheries in freshwater habitats, coastal zones, and island archipelagos (Bouchet et al., 1999, 2001; Hoberg et al., 2012). Diphyllobothrium latum in particular appears to be primarily a parasite of people and historical occurrence of this spe-cies in North America may reflect both late Pleistocene expansion across Beringia, and later anthropogenic introductions associated with European exploration and colonisation establishing focal distributions in the eighteenth century resulting in a faunal mosaic (Dick, 2008; Hoberg et al., 2012; Rausch and Hilliard, 1970).

Life cycles for diphyllobothriids are complex, involving one crusta-cean and at least two vertebrates, generally a fish and a piscivorous avian or mammalian definitive host (Adams and Rausch, 1997; Dubinina, 1966) (Fig. 2.19). Among diphyllobothriids (zoonotic species of Diphyllobothrium, Diplogonoporus, Pyramicocephalus, and Schistocephalus considered here), adult tapeworms inhabit the small intestine of definitive hosts and release eggs that are passed in host faeces. In marine environments, eggs have thick, pitted shells, while in freshwater, eggs have thin, nonpitted shells (Hilliard, 1960). Eggs hatch in water to release a coracidium (ciliated oncosphere), which is ingested by diaptomid or cyclopid copepods serving as first IHs. Procercoid larval stages develop within the copepod, which is subsequently ingested by a zooplanktivorous fish serving as a second IH. Within the fish, development to the plerocercoid larval stage occurs either in the viscera or musculature; plerocercoids may be encapsulated or free in the peritoneal cavity depending on the species (Scholz et al., 2009). Infection of birds or mammals may occur at this juncture through predation of infected fishes, or further dissemination of parasites may involve circulation among PHs,


Arctic Zoonoses 123


often larger predatory piscivorous fishes, which are most often the source of human infection. The predilection site and behaviour of plerocercoids in different hosts and tissues influences both geographic distribution for assemblages of hosts and parasites, and potential sources for human infections. Zoonotic and non-zoonotic species of diphyllobothriids may circulate among mammalian, avian, and fish hosts in the same region (Table 2.13), rendering species-level identifications critical to assessing human risk (Andersen et al., 1987; Curtis and Bylund, 1991; Curtis et al., 1988; Rausch and Hilliard, 1970).

There are four potential pathways for transmission of diphyllobothriids in marine and freshwater environments (Table 2.13; Fig. 2.19). (1) Strictly freshwater cycles, such as those for Diphyllobothrium dalliae, D. dendriticum, D. latum and Schistocephalus solidus utilise freshwater fishes and piscivo-rous birds or terrestrial mammals as definitive hosts, depending on the species involved. (2) Strictly marine cycles, including those for D. cordatum, D. pacificum, D. hians and species of Diplogonoporus, involve marine mammals

Figure 2.19 Simpli!ed, generic life cycle of diphyllobothriid cestodes (such as Diphyllo-bothrium latum) in marine and freshwater cycles in the North. Adult cestodes are pres-ent in the intestine of de!nitive hosts, including people, dogs, and pisicivorous wildlife. De!nitive hosts become infected by consumption of !sh intermediate (IH) or paratenic hosts (PH).



124


Table 2.13 Location and Host Distribution for Diphyllobothriidae, Including Zoonotic Species of Diphyllobothrium, Diplogonoporus, Pyramicocephalus, and Schistocephalus at high latitudesSpecies Location Fish Hosts De!nitive Hosts Transmission Reference

Diphyllobothrium spp.

D. alascense Western AK Burbot (Lota lota), Boreal smelt (Osmerus mordax), Diadromous forage fishes

Dog (Canis lupus familiaris), Human

Marine-Freshwater

Rausch and Wil-liamson (1958); Rausch et al. (1967); Rausch and Adams (2000)

D. cordatum Circumpolar Unknown Phocid seals (Phoca spp.), Bearded Seal (Erignathus barbatus), Walrus (Odobenus rosmarus), Dog, Human

Marine Leuckart (1863); Markowski (1952); Rausch et al. (1967); Rausch (2005)

D. dalliae Western AK, Eastern Chukhotka, AK

Blackfish (Dallia pectoralis), Dolly Varden (Salvelinus malma)

Dog, Arctic Fox (Vulpes lagopus), Human, Laridae (Larus spp.)

Freshwater Rausch (1956a); Rausch and Hilliard (1970)

D. dendriticum Circumpolar Salmonidae (Salmoninae, Coregoninae), Gasteros-teidae, Burbot

Piscivorous birds (Laridae), Terrestrial mammals, Human

Freshwater Rausch and Hilliard (1970); Andersen et al. (1987); McDon-ald and Margolis (1995); Dick (2008); Scholz et al. (2009)

D. ditremum Holarctic (Boreal) Salmonidae, Gasteroste-idae, Osmeridae

Piscivorous birds Freshwater Andersen et al. (1987)


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D. fayi Bering Sea, Arctic Ocean

Unknown Pacific Walrus Marine Rausch (2005)

D. hians Circumpolar Unknown Ringed Seal (Phoca hispida), Bearded Seal, Northern Fur Seal (Callorhinus ursinus), Human

Marine Scholz et al. (2009)

D. lanceolatum Circumpolar Least cisco (Coregonus sardinella)

Bearded Seal, Harbour Seal (Phoca vitulina), Ringed Seal, Ribbon Seal (Phoca fasciata), Dog, Human

Marine-Freshwater

Markowski (1952), Rausch and Hilliard (1970)

D. latum Holarctic, Temperate to Sub-Arctic

Esocidae, Percidae, Burbot, Cottidae, Salmonidae

Human, Terrestrial mammals

Freshwater Plotnikof (1935); Rausch et al. (1967); Rausch and Hilliard (1970); Deliamure et al. (1985); Dick (2008); Scholz et al. (2009); Hoberg et al. (In Press)

D. nihonkaiense N. Pacific basin, coastal/boreal

Salmonidae (Onchorhyn-chus spp.)

Brown Bear (Ursus arctos), Human

Freshwater-Marine

Scholz et al. (2009)

Continued



126


D. pacificum Pacific Basin, Temperate Northern/ Southern Hemisphere

Unknown Otariidae: Northern Fur Seal, Steller Sea Lion (Eumetopias jubatus), California Sea Lion (Zalophus californianus), Juan Fernandez Fur Seal (Arctocephalus philippi), Human

Marine Rausch et al. (2010), Scholz et al. (2009); Rausch et al. (2010)

D. orcini North Pacific basin Unknown Killer whale (Orcinus orca), Human

Marine Kamo (1999); Scholz et al. (2009)

D. roemeri Arctic Basin Unknown Walrus Marine Schmidt (1986), Kamo (1999)

D. skrjabini Greenland, Bering Strait

Unknown Bearded seal Marine Iurakhno and Mal’tsev (1993)

D. stemmaceph-alum

Holarctic, boreal Unknown Delphinidae, Human Marine Scholz et al. (2009)

D. ursi NE Pacific, coastal/boreal-sub-Arctic

Red salmon (O. nerka) Pacific salmon (Oncho-rhynchus spp.)

Bear (U. arctos, U. americanus), Human

Freshwater-Marine

Rausch (1954); Rausch and Hilliard (1970)

Table 2.13 Location and Host Distribution for Diphyllobothriidae, Including Zoonotic Species of Diphyllobothrium, Diplogonoporus, Pyramicocephalus, and Schistocephalus at high latitudes—cont’dSpecies Location Fish Hosts De!nitive Hosts Transmission Reference


Arctic Zoonoses127


Diplogonoporus spp.

D. balae-nopterae

Circumpolar Engraulidae, Clupeidae Japanese Anchovy (Engraulis japonica) Japanese Sardine (Sardinops melanostictus)

Baleen Whales, Human, Dog

Marine Rausch (1964); Adams and Rausch (1997); Scholz et al. (2009); Arizono et al. (2008)

D. tetrapterus North Pacific basin Unknown Sea Otter (Enhydra lutra), Northern Fur Seal, Steller Sea Lion

Marine Margolis (1956); Rausch (1964)

D. violettae Bering Sea Unknown Steller Sea Lion Marine Iurakhno (1986)

Pyramicocephalus spp.

P. phocarum Circumpolar Marine fishes, nearshore, demersal, Cottidae, Gadidae

Phocid seals, Human Marine-freshwater

Rausch and Hilliard (1970); Deliamure et al. (1985); Rausch and Adams (2000)

Schistocephalus spp.

S. solidus Circumpolar Nine-spined Stickleback (Pungitius pungitius)

Piscivorous Birds, Mammals, Human

Freshwater Rausch et al. (1967); Dubinina (1966)

Abbreviations for states, provinces, and territories as in Fig. 2.1.




and fishes in nearshore and oceanic habitats. (3) Marine-to- freshwater cycles, such as those for Diphyllobothrium alascense, D. lanceolatum, and Pyramico-cephalus, occur when marine mammals indirectly infect diadromous for-age fishes in the marine environment. For example, for D. lanceolatum and D. alascense from western Alaska and Chukhotka, coracidia expelled by pinniped definitive hosts result in plerocercoid infections in migratory forage fishes including some osmerids and coregonids (but not appar-ently salmonids) that serve as prey for freshwater PHs (Rausch and Adams, 2000; Rausch and Hilliard, 1970). Although cycles are initiated in marine environments, transmission to dogs and humans apparently often occurs through ingestion of infected fishes in freshwater. (4) Freshwater- to-marine cycles, such as those for D. ursi and D. nihonkaiense, occur when brown bears (U. arctos) indirectly infect salmon IHs ( species of Onchorhynchus) in freshwater environments prior to the migration of smolt downstream to the ocean. Mature spawning salmon returning to natal streams carry infective plerocercoids and life cycles are completed when foraging bears (or humans) take these fish as prey (Rausch, 1954; Rausch and Hilliard, 1970).

It is apparent that several mechanisms are associated with transfer of marine diphyllobothriids and other helminths (such as anisakid nematodes) into freshwater transmission cycles: (1) consumption of marine fishes by freshwater piscivores transiently moving into estuarine/brackish water; (2) consumption of marine fishes ascending a short distance into freshwater environments; and (3) consumption of anadromous fishes ascending into lotic (moving water; e.g. river) and lacustrine (e.g. lake) systems to spawn (Rausch and Adams, 2000). For D. alascense and Pyramicocephalus, some spe-cies of freshwater predatory fishes such as burbot (Lota lota) appear to be important in facilitating linkages between the marine and lotic environ-ments (Rausch and Adams, 2000). Interacting factors related to piscine and homeotheric hosts, ecological context, and tolerance and resilience to tem-perature and salinity during life history stages for these parasites serve to determine the potential for human infection.

9.1. Species Present in the NorthThe most common zoonotic diphyllobothriid species in the Northern Hemisphere are D. latum and D. dendriticum (Curtis and Bylund, 1991; Lan-tis, 1981; Yera et al., 2006). Among the approximately 50 recognised species of Diphyllobothrium, relatively few are known to occur at high latitudes, and even fewer are restricted in distribution to the sub-Arctic and Arctic


Arctic Zoonoses 129


(Adams and Rausch, 1997; Deliamure et al., 1985; Scholz et al., 2009). Although the overall diversity for zoonotic diphyllobothriids remains to be completely resolved, globally 17 species (excluding species of Spirometra in Asia and the tropics) have been identified in association with human infec-tions (Adams and Rausch, 1997; Deliamure et al., 1985; Dick, 2008; Rausch et al., 1967; Scholz et al., 2009). Among these, 15 species in terrestrial and marine piscivores (including Diplogonoporus balaenopterae, Pyramicocephalus phocarum, and S. solidus) have been documented in people across the circum-polar north or in adjacent seas extending southward into boreal latitudes of the North Pacific basin, including Japan and the North (Table 2.13). Lati-tudinal gradients in diversity appear evident, with greatest species’ richness in the sub-Arctic and temperate zones, with few species being restricted to the Arctic (Deliamure et al., 1985; Dick, 2008; Rausch and Hilliard, 1970; Scholz et al., 2009). Greenland has a particularly depauperate community of diphyllobothriids, at least in terrestrial carnivores (Babbott et al., 1961; Leuckart, 1863).

9.2. Geographic Distribution in the NorthDiphyllobothriid cestodes are present in marine and freshwater systems across the North. Some species have relatively limited geographic dis-tributions (D. alascense and D. dalliae in western Alaska; D. nihonkianese, D. pacificum, and D. ursi in the coastal North Pacific), whereas others exhibit circumpolar distributions (D. dendriticum, D. latum, D. lanceola-tum, and P. phocarum) (Table 2.13). Such associations reflect ecologically defined patterns of transmission, mobility, and migratory behaviour of fish, bird, and mammal hosts, and historical events of range expansion and isolation (Hoberg et al., 2012). Anthropogenic translocations into North America include introduction with immigrants across Beringia in the late Pleistocene, and more recent introductions with European explora-tion and contact since the eighteenth century (Adams and Rausch, 1997; Bouchet et al., 1999, 2001; Dick, 2008; Hoberg et al., 2012; Rausch and Hilliard, 1970).

Diphyllobothrium latum and D. dendriticum are distributed across boreal to sub-Arctic North America (Fig. 2.20). Diphyllobothrium dendriticum, how-ever, appears to be the dominant species north of 60°N in Canada and Alaska (Dick, 2008), and may be the only species present in aquatic/ter-restrial systems in Greenland (Kapel and Nansen, 1996; Rausch et al., 1983). Plerocercoids of D. latum have been reported in fishes up to 61°N in the Northwest Territories, as well as in northern Manitoba, Saskatchewan, and




Alberta (Ching, 1984; Dick, 2008; Dick and Poole, 1985; Dick et al., 2001), and are present near the Arctic Circle (ca. 66°N) in Alaska (Rausch and Hilliard, 1970).

Confusion about the distribution of D. latum in North America and elsewhere has resulted from uncritical application of this name to diphyl-lobothriids in humans and other mammals, absence of morphologically identified specimens for comparison, and diagnoses based solely on eggs in faecal samples (Adams and Rausch, 1997; Dick, 2008). The extraordi-nary host range reported for D. latum by Deliamure et al. (1985) requires confirmation (Scholz et al., 2009; Yera et al., 2006). The application of molecular-based methods holds great promise to identify eggs in faecal samples, morphologically similar adult tapeworms in birds and mammals, and plerocercoid larvae in marine and freshwater fishes. Resolution of the actual host and geographic range for D. latum must be established through examination of adult cestodes and/or development of accurate molecular foundations for identification and differentiation among morphologically similar cestodes.

Figure 2.20 Published reports of diphyllobothriid cestodes in animals and people in Alaska, northern Canada, and Greenland. (Data from Tables 2.14 and 2.15).


Arctic Zoonoses 131


9.3. Transmission, Prevalence, and Animal Health Impact in the North9.3.1. Prevalence in Terrestrial PiscivoresReports of diphyllobothriids in domesticated and free-ranging terrestrial carnivores across the North are predominately based on the presence of characteristic eggs in faeces; in relatively few situations have adult cestodes been examined or identified, nor have molecular techniques been applied to surveys of wild and domestic carnivores in the North (Table 2.14). Thus, substantial gaps may exist in our basic understanding about host associa-tions, geographic distribution, and species diversity (Dick, 2008). Histori-cally, prevalence in dogs has approached 50% in settlements adjacent to marine or freshwater habitats. Fish are often a dietary mainstay for north-ern dogs (Canis familiaris) (Rausch and Hilliard, 1970; Salb et al., 2008). Terrestrial wild canids and bears are hosts for various diphyllobothriids; however, prevalence in wild canids tends to be considerably lower than in dogs (Table 2.14). This may reflect seasonal and geographical variation in the proportions of marine, freshwater, and anadromous fishes and other wildlife represented in the diet (Cameron et al., 1940; Kapel and Nansen, 1996; Rausch and Hilliard, 1970). Diphyllobothrium spp. cestodes were not detected in 200 wolves (C. lupus) from the Copper River drainage, nor in 80 wolverine (G. gulo) from the Susitna River drainage and the Brooks Range of Alaska in 1949–1959 (Rausch, 1959a; Rausch and Williamson, 1959).

A similar spectrum of fish shared in diets of domestic dogs and people indicates that parasite faunas may have considerable overlap with respect to species’ richness and diversity (Rausch and Hilliard, 1970; Rausch et al., 1967). Demonstration of parasite diversity in canine populations has been shown to be an accurate proxy with respect to the range of hel-minth parasites likely to be derived by people from fishes in marine or freshwater environments (Rausch and Hilliard, 1970; Rausch et al., 1967). Indeed, in many remote and indigenous communities, free-ranging dogs and sled dogs are often at higher risk of exposure than people (due to consumption of uncooked fish) and may serve as excellent sentinels for the presence of potentially zoonotic species of Diphyllobothrium ( Jenkins et al., 2011; Rausch and Hilliard, 1970; Salb et al., 2008). For example, in two communities in northern Quebec (Nunavik), only two of 87 people were positive (Curtis et al., 1988), whereas concurrently 45% of 80 dogs were shown to be shedding eggs of Diphyllobothrium spp. (Desrochers and Curtis, 1987).



132


Table 2.14 Prevalence [% (n)] of Diphyllobothrium spp. in Representative Terrestrial and Marine Piscivores

Host Location(s)Prevalence[% (n)]

Parasite Identi!cation Method References

Order Carnivora

Arctic Fox St. Lawrence Island, AK 3 (1579) D. dendriticum N Rausch et al. (1990a)(Vulpes lagopus) St. Matthew Island, AK 32 (22) D. dendriticum,

D. dalliaeN Rausch and Rausch (1968);

Rausch and Hilliard (1970)Brooks Range, AK 1 case D. latum N Rausch and Hilliard (1970)Greenland 10 (38) D. dendriticum N Rausch et al. (1983)8 sites, Greenland 6–15* (254) D. dendriticum N Kapel and Nansen (1996)

Black Bear (Ursus americanus)

Prince of Wales Island, AK 1 case D. ursi N Rausch and Hilliard (1970)

Valdez Island, AK 1 case D. ursi N Rausch and Hilliard (1970)Peace River, AB 1 (91) NR N Dies (1979)

Brown Bear (Ursus arctos)

Karluk Lake, Kodiak Island, AK

1 case D. ursi N Rausch (1954)

Taku River Valley, BC and YT

14 (21) NR N Choquette et al. (1973)

Daring Lake, NT 18 (56) NR FF Gau et al. (1999)Dog (Canis familiaris) Kotzebue, AK 1 (97) D. latum N Rausch and Hilliard (1970)

Western Alaska; Yukon-Kuskokwim Delta

59 (97) D. alascense, D. dalliae, D. dendriticum, D. lanceolatum

N Rausch et al. (1967); Rausch and Hilliard (1970)

Assumption, AB; Fort Liard, Fort Rae, and Snowdrift, NT

35 (327) D. latum FF, N Unruh et al. (1973)

Fort Resolution, NT and Fort Chipewyan, AB

7 (129) NR FF Salb et al. (2008)


Arctic Zoonoses133


Fort Chipewyan, AB 47 (88) NR FS Saunders (1949)Fox Lake, AB 6 (272) NR FF Unruh et al. (1973)13 sites in SK 3 (3370) NR FF Allen and Mills (1971)Loon Lake, La Ronge, SK 10 (106) NR FF Unruh et al. (1973)29 sites in NT, AB, SK,

MB, NU, QC, NLNR NR FF Cameron et al. (1940)

Wolstenholme, QC and Nottingham, NU

NR Diphyllobothrium spp.

N Cameron et al. (1940)

Kuujjuaq, QC 45 (80) NR FF Desrochers and Curtis (1987)

Greenland NR D. cordatum N Krabbe (1868)Red Fox

(Vulpes vulpes)Ambler, AK 1 case D. latum N Rausch and Hilliard (1970)

Wolf (Canis lupus) Thelon River, NT 2 (61) Diphyllobothrium N Choquette et al. (1969)

Order Pinnipedia

Bearded Seal Bering Sea, AK and Sea of Okhotsk, 4 sites

0–21* (82) Diphyllobothriidae N Adams (1988)(Erignathus barbatus) 0–30* (82) Diphyllobothrium N Adams (1988)

30–100* (82) D. lanceolatum N Adams (1988)0–60* (82) Pyramicocephalus

phocarumN Adams (1988)

Northern Fur Seal (Callorhinus ursinus)

Northern Bering Sea NR D. pacificum N Rausch et al. (2010)

Ringed Seal (Phoca hispida)

Hudson Strait, Salluit, QC

80 (5) Diplogonoporus tetrapterus

N Measures and Gosselin (1994)

10 sites, Bering Sea to Arctic coast, AK

0–33* (299) Diphyllobothrium N Adams (1988)0–40* (299) Diplogonoporus N Adams (1988)0–39* (299) P. phocarum N Adams (1988)

Continued



134


Ribbon Seal Central Bering Sea, AK 6 (31) D. cordatum N Shults and Frost (1988)(P. fasciata) Central Bering Sea, AK 3 (31) D. lanceolatum N Shults and Frost (1988)Spotted Seal Bering Sea, AK 24 (55) D. tetrapterus N Shults (1982)(P. largha) Bering Sea, AK 20 (55) D. cordatum N Shults (1982)

Anadyr, Bering Sea 2 (130) Diphyllobothrium N Deliamure et al. (1984)Pribilof Island, AK 7 (57) Diphyllobothrium N Deliamure et al. (1984)

Steller Sea lion Bering Sea, AK 94 (67) D. tetrapterus N Shults (1986)(Eumetopias jubatus) Gulf of Alaska, AK 28 (7) D. tetrapterus N Shults (1986)

Bering Sea, AK 31 (67) D. pacificum N Shults (1986)Gulf of Alaska, AK 14 (7) D. pacificum N Shults (1986)

Walrus North Pacific/Bering Sea, 3 sites, AK

2–10* (306) D. cordatum N Adams (1988)(Odobenus rosmarus) 0–2* (306) D. lanceolatum N Adams (1988)

1–10* (306) D. roemeri N Adams (1988)Chukchi Sea, AK 10 (95) D. fayi N Rausch (2005)

Within a host species, reports move from west to east across the North. Abbreviations for states, provinces, and territories as in Fig. 2.1.N – Necropsy, NR – Not recorded, FF– Faecal flotation, FS – Faecal smear.*Range of site-specific prevalences.

Table 2.14 Prevalence [% (n)] of Diphyllobothrium spp. in Representative Terrestrial and Marine Piscivores—cont’d

Host Location(s)Prevalence[% (n)]

Parasite Identi!cation Method References


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Diphyllobothrium spp. are thought to have little impact on the health of mammalian definitive hosts, although there is a report of blockage of the pancreatic duct in a captive black bear (U. americanus) in Alaska (Rausch, 1955). In fish, plerocercoids may be associated with pathology and may have a detrimental influence on palatability and suitability of some piscine species as food (reviewed in Marcogliese, 2001).

9.3.2. Prevalence in Marine PiscivoresAlthough multiple genera and species of diphyllobothriids circulate among pinnipeds and cetaceans, it is generally those species in pinnipeds (seals, sea lions, and walruses) that have been shown to be zoonotic (Tables 2.13 and 2.14) (Deliamure et al., 1985; Kamo, 1999; Scholz et al., 2009). Diphyllo-bothriids are not known in polar bears (U. maritimus), and this may reflect a specialised diet of seals and carrion and associations with ice edge and pack ice habitats. The apparent propensity of zoonotic species to circu-late among pinnipeds may be indicative of linkages within near-shore food webs, relatively focal sources due to breeding distributions and haul-outs, and frequent involvement of large piscine prey (potential PH) that represent a food resource for both marine mammals and people. For example, spotted seals (Phoca largha) are generally associated with sea ice of the Bering Sea during parturition early in the spring, but disperse into nearshore, coastal, and estuarine habitats later in the summer (Deliamure et al., 1984). Among species of pinnipeds, diphyllobothriids are often the most prevalent and abundant tapeworms, and multiple species infections are not uncommon (Table 2.14) – 11 species parasitise pinnipeds, with six being zoonotic (Table 2.13). In contrast, only three species with cetacean definitive hosts, Diphyl-lobothrium orcini in killer whales (Orcinus orca) that specialise on salmonids, Diphyllobothrium stemmacephalum in small delphinids, and D. balaenopterae in baleen whales, are known in zoonotic infections (Deliamure et al., 1985; Kamo, 1999).

9.4. Transmission, Prevalence, and Public Health Impact in the NorthHumans become infected with diphyllobothriid cestodes through consumption of plerocercoids in fish IHs or PHs, and thus serve as definitive hosts with adult cestodes in the small intestine. Transmission to people occurs where fresh, undercooked fish (and possibly smoked, dried, fermented, or salted fish) are consumed for cultural and nutritional reasons (Adams and Rausch, 1997; Gyorkos et al., 2003; Rausch and Hilliard, 1970;




Rausch et al., 1967). In some communities, locally caught fish compose approximately a third of all harvested country foods (Mackey, 1988; Ross et al., 1989). Diphyllobothriid species in which plerocercoids localise in the skeletal muscle (or migrate from the viscera into the muscle following death of the fish) are more likely to be consumed by people. For example, the usual predilection site for plerocercoids of D. ursi in the viscera may preclude extensive infections in people, although at some localities such as Kodiak Island, AK, nearly all returning salmon may be infected (Adams and Rausch, 1997). In addition, Indigenous Arctic residents in some regions consume the stomach and liver of fish (Ross et al., 1989). Plerocercoids may have a detrimental influence on suitability and palatability of dietary fish, although levels of traditional knowledge about the life cycle and sig-nificance of this group of cestodes vary. Dogs and wild carnivores are not a direct source of human exposure but may serve to amplify local cestode populations if faeces are deposited near water (Adams and Rausch, 1997; Scholz et al., 2009).

Most diphyllobothriids have zoonotic potential; only six of the 21 diphyllobothriid species distributed in northern environments of the Western Hemisphere have not been documented in people (Table 2.13). These associations indicate that the potential for dissemination to people is strongly controlled by local ecology and fisheries. Only two diphylloboth-riid species, D. dendriticum and D. latum, are commonly reported in people; other species and genera of diphyllobothriids appear to be incidental in people and companion animals such as dogs. Across Alaska, where there is a diverse assemblage of species of Diphyllobothrium, records of D. latum are almost always limited to infections in people (Rausch and Hilliard, 1970) (Table 2.15). The diversity of other diphyllobothriids in people reflects dif-ferences in local cycles, dietary preferences, and distributions for primary definitive host species (Adams and Rausch, 1997; Rausch and Hilliard, 1970; Rausch et al., 2010). With the potential exception of D. latum, species of Diphyllobothrium are maintained in endemic transmission cycles usually independent of people as obligate definitive hosts. Consequently, diphyllo-bothriosis can be regarded as a natural focal infection at landscape scales that cannot simply be controlled by elimination of cestodes from the human population (Adams and Rausch, 1997).

Transmission of diphyllobothriids in human communities appears to be largely limited to isolated settlements scattered across northern latitudes (Rausch, 1974). In Greenland, human infections with diphyllobothriids appear to be rare; although D. cordatum has been reported (Leuckart, 1863),


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Table 2.15 Prevalence [% (n)] of Diphyllobothriosis in People Based on Detection of Eggs in Faeces and/or Identi!cation of Adult Cestodes

Location Sampling DatesPrevalence [% (n)] Identity References

Alaska, USA

Lower Kuskokwim River 1949 15 (100) Diphyllobothrium sp.* Hitchcock (1950)Kotzebue 1950 6 (100) Diphyllobothrium sp.* Hitchcock (1951)Hooper Bay 1957–1958 22 (1299) D. cordatum, D. alascense,

D. dalliaeRausch et al. (1967)

Chevak, Newtok, Nelson Island 1958 NR Schistocephalus solidus Rausch et al. (1967)Southwestern Alaska 1958 11 (1680) Diphyllobothrium sp.* Fournelle et al. (1958)Yukon-Kuskokwim Delta 1949–1970 NR D. alascense, D. dalliae,

D. dendriticum, D. lanceolatum†

Rausch and Hilliard (1970)

Kodiak Island/Ft. Yukon 1970 NR D. ursi † Rausch and Hilliard (1970)Western Alaska (multiple villages) 1949–1970 53 (34) D. latum† Rausch and Hilliard (1970)Fairbanks, Anchorage, Bethel, and

Haines1981 6 cases D. latum‡ Alaska Epi. Bull. (1981)

King Salmon 1984 7 confirmed cases, 11 ill

D. latum‡ Alaska Epi. Bull. (1984)

Canada

Fort Chipewyan, AB 1945 11 (140) Diphyllobothrium sp.* Saunders (1949)Southampton Island, NU 1947 29 (31) Diphyllobothrium sp.* Brown et al. (1948)Igloolik, NU 1949 33 (97) Diphyllobothrium sp.* Brown et al. (1950)MB, NT, ON, QC 1953 11.5 (426) Diphyllobothrium sp.* Wolfgang (1954)Kuujjuaq, QC, (Ft. Chimo) 1959 28 (46) Diphyllobothrium sp.* Laird and Meerovitch (1961)

Continued



138


Location Sampling DatesPrevalence [% (n)] Identity References

Inukjuaq, QC (Port Harrison) 1960 77 (328) Diphyllobothrium sp.* Arh (1960)Igloolik, NU 1970–1971 2 (247) Diphyllobothrium sp.*,

D. dendriticum**Freeman and Jamieson

(1976)Northern Ontario 1974–1975 1.7 (536) Diphyllobothrium sp.* Watson et al. (1979)Kuujjuaq, QC 1986 2 (87) Diphyllobothrium sp.* Curtis et al. (1988)Greenland 1863 NR Diphyllobothrium cordatum Leuckart (1863)

Reports move from west to east, then chronologically within a state, province, or territory. Abbreviations for states, provinces, and territories as in Fig. 2.1.NR – Not recorded.*Identification of eggs in faeces possible only to genus level.†Based on morphological identification of strobilate adults recovered from naturally infected people.‡Associated with consumption of raw salmon; diphyllobothriid species identification uncertain. See: http://www.epi.alaska.gov/bulletins/docs/b1981_22.htm http://www.epi.alaska.gov/bulletins/docs/b1984_19.htm**Based on morphological identification of strobilate adults recovered from experimentally infected human volunteer.

Table 2.15 Prevalence [% (n)] of Diphyllobothriosis in People Based on Detection of Eggs in Faeces and/or Identi!cation of Adult Cestodes—cont’d




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no eggs were detected in 670 faecal samples from people in the Disko Bay region tested in 1957 (Babbott et al., 1961). Diphyllobothriosis was common among indigenous populations of Canada and Alaska into the middle of the last century (prevalence generally around 30%, as high as 83%), but appears to have declined in the following decades (Gyorkos et al., 2003). For example, in Igloolik in the eastern Canadian Arctic, prevalence dropped from 33% in 1949 to 2% in 1970–1971, and in Kuujjuaq, preva-lence dropped from 28% in 1959 to 2% in 1986 (Table 2.15). Prevalence elsewhere in Canada appeared to be low (about 11%) in the 1940s and 1950s, and may also be declining. Between 1969 and 1978, 46 cases were reported from the NT and what is now Nunavut, whereas between 1995 and 1998, only five cases of ‘tapeworm’ (either Diphyllobothrium or Echino-coccus granulosus) were reported to territorial public health authorities.

During the 1960s in western Alaska, diphyllobothriosis was common (up to 30% peaking in late winter or spring) and reflected seasonal diets that by necessity were rich in small forage fishes such as pond smelt, blackfish, and sticklebacks, which were often eaten partially frozen or raw (Rausch et al., 1967). In contrast, prevalence was considerably lower in late summer (16%), coinciding with opportunities for a more diversified diet. More recently, individual cases or localised outbreaks at various localities in Alaska during the early 1980s have been associated with consumption of raw or undercooked salmon (Table 2.15). Overall, incidence appears to be decreasing in the general North American population (Scholz et al., 2009); however, surveillance is limited as diphyllobothriosis is not report-able to public health authorities at the national level in North America. In addition, factors hindering detection include reticence to report passing of cestodes to medical personnel and to submit faecal samples for testing. Declining levels of infection in people may reflect changes in traditional diets over the past 50–60 years.

Diphyllobothriosis is rarely associated with detectable clinical disease in North America. Pernicious anaemia associated with D. latum in Finland appears to have a complex aetiology involving interactions among genetic susceptibility and poor nutrition. This syndrome is seldom observed in recent times, even in Finland, and has never been clinically prominent in Canada or North America (Curtis and Bylund, 1991; Rausch et al., 1967). Other species of Diphyllobothrium likely cause no or transient gastrointesti-nal signs. Duration of infection with D. dendriticum is generally only four to six months (Curtis and Bylund, 1991), although strobilate adults of D. latum may persist for decades.




Globalisation of trade and rapid transport of fresh fish may lead to resur-gence for diphyllobothriosis in people, even at sites far distant from local transmission cycles for these parasites in the north. For example, the recogni-tion of D. nihonkaiense as a zoonotic parasite from western North America was based on molecular identification of proglottids passed by a patient in France following the consumption of raw salmon (presumed to be Oncorhynchus keta) from the Gulf of Alaska (Yera et al., 2006). Additional human infections for species of Diphyllobothrium in western Europe have been related to impor-tation of exotic fish (e.g. species of Pacific salmon) and new cuisines that emphasise fresh and raw ingredients (Scholz et al., 2009). In addition, import-ing new customs into the North may lead to localised outbreaks; in an out-break in Alaska in 1984, the suspected source of infection was locally caught salmon prepared using a recipe for ceviche brought to Naknek by a visitor from California (http://www.epi.alaska.gov/bulletins/docs/b1984_19.htm).

9.5. Diagnosis and ControlDiagnostic identification of strobilate (adult) diphyllobothriids in infections of definitive hosts (people, mammals, and birds) can be achieved through morphological or molecular means (Rausch and Hilliard, 1970; Scholz et al., 2009; Yera et al., 2006). Diagnostic criteria have been well character-ised for the genera and species recognised as zoonotic and for most species that occur in terrestrial, aquatic, and marine piscivores (Deliamure et al., 1985; Rausch et al., 2010). In patent infections, diphyllobothriosis in people is still most often diagnosed based on the discovery of typical segments or eggs in faeces, and such basic procedures are rapid and inexpensive. Recov-ery of intact adults, however, remains the only established morphological means for determining identity, but specimens must be in good condition, and should retain the scolex to facilitate this process. Unfortunately many human infections have simply been identified as D. latum by default.

Identification of infective plerocercoids in fish IHs and PHs continues as a challenge, although for some species these larval stages are morphologically distinct (Rausch and Hilliard, 1970). For example plerocercoids of D. ditremum, D. dendriticum and D. latum circulating in freshwater fishes can often be rec-ognised (Andersen and Gibson, 1989), and metacestodes of Pyramicocephalus and D. lanceolatum in brackish and marine habitats are distinctive (Rausch and Adams, 2000; Rausch and Hilliard, 1970). Application of molecular-based methodologies has increasingly allowed many of these tapeworms to be differ-entiated at the generic and species level, as sequence data across the assemblage of diphyllobothriids continues to be developed (Scholz et al., 2009). Overall,



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these methods, based on either nuclear or mitochondrial DNA sequences, are the most reliable tools for specific identification, and are appropriate for all developmental stages in DHs, PHs, and IHs. Even though the apparent clini-cal significance of diphyllobothriosis in people is often limited, specific iden-tification remains important as a tool in epidemiology and in tracking the sources of human infection at both local and regional scales. Such has become increasingly important given the rapid and global transport and dissemination of infected fish consumed in urban centres throughout the world.

Control of diphyllobothriosis is dependant on breaking the cycle for trans-mission and can be achieved through treatment of infected people and dogs, eliminating contamination of water sources (with human sewage treatment especially relevant for D. latum), and limiting access to salmoniforms and other fishes that harbour infective plerocercoids (Adams and Rausch, 1997; Rausch et al., 1967; Scholz et al., 2009). Protocols for treatment are now well estab-lished, and adult tapeworms are highly susceptible to either praziquantel or niclosamide administered orally in well-determined dosage regimes (Scholz et al., 2009); in dogs, it is important to note that the dose of praziquantel is higher than that routinely used to eliminate other cestode infections. Reduc-ing or eliminating exposure through safe food preparation practices, such as adequate cooking of potentially infected fishes, are the most effective means of prophylaxis. Fishes that are consumed raw, smoked, or pickled should first be frozen for several days at minus 10 °C or colder to kill infective plerocercoids.

As noted, shifting diets for indigenous peoples in the north have tended to reduce the levels of exposure and infections for species of Diphyllbothrium over the past several decades. Salmon, however, continue to pose a risk of human infection well beyond the borders of northern regions, and far from the locali-ties where transmission is endemic for a number of species, including D. ursi and Diphyllobothrium nihonkaiense. As Scholz et al. (2009) noted: ‘Salmon are now transported worldwide only on ice, and this is the way that fish helminths are usually introduced to new areas and may infect humans anywhere.’ Thus interventions to limit the distribution of human infections by diphyllobothriids must also involve education and discussion of the risks of consumption of raw fish both across the villages of the north and in urban centres around the world.

9.6. Future Impact of Climate and Landscape ChangeClimate warming and associated ecological perturbations are modifying the structure of terrestrial, freshwater, and marine systems across high latitudes of the north and globally (Burrows et al., 2011; Callaghan et al., 2004; Gilg et al., 2012; Hoberg et al., in press; Post et al., 2009). For diphyllobothriids,




these changes will have an effect on patterns of distribution, seasonal tim-ing of migration and reproduction of definitive hosts, and development and survival of fish hosts (second IHs and PHs), invertebrate first IHs, and free-living parasite stages (eggs and coracidia). Interactions and linkages between abiotic and biotic drivers that unfold in terrestrial, freshwater, and marine systems may fundamentally alter the distribution and abundance of diphyllobothriids in the North.

In northern freshwater systems, current predictions suggest that fish-ing practices, eutrophication, and temperature increases may have the most profound effects on freshwater fish and their parasites (Marcogliese, 2001, 2008). Overall, freshwater systems are highly sensitive to water levels, ice cover, flow rates, and changing patterns of primary and secondary produc-tivity that influence ecosystem structure and potential prey diversity and abundance for fish, birds, and some mammals (Marcogliese 2001, 2008). These factors are central to the continuity of life cycles and potential for transmission of Diphyllobothrium and Schistocephalus spp. The effects of cli-mate change on diphyllobothriids in freshwater systems may be manifested by: (1) shifts in development for invertebrates that involve tipping points or transitions in life history from multiple to single-year cycles; (2) loss of cold-water refugia leading to range reductions and extirpation of fishes and their parasites endemic to the Arctic when tolerances and resilience are exceeded; (3) changing distribution of wetland habitats; (4) northward extension of the ranges for many host species (such as yellow perch, Perca flavescens, and invertebrates) leading to introductions of parasite species pre-viously unknown in the north (Reist et al., 2006); and (5) higher diversity for fish and invertebrates (Schindler and Smol, 2006). For example, given the current low diversity of freshwater diphyllobothriids in Greenland, climate change may allow establishment of exotic species, if introduced through anthropogenic translocation or movements of migratory hosts.

For diphyllobothriids currently common in freshwater systems in the North (D. latum and D. dendriticum), environmental change will influence the patterns of transmission and distribution. Increasing water temperatures and expanded periods for ice-free conditions may relax biotic and abiotic con-trols on the distribution of D. latum, which currently appears to be restricted to the sub-Arctic and boreal zones ( Jenkins et al., 2011). If a different set of fish second IH expands northward, this will represent new sources of human infection in freshwater systems. Further, temperature has direct effects on the development of D. dendriticum in the environment and in both invertebrate and piscine IH. For example, warmer temperatures accelerate embryonation


Arctic Zoonoses 143


and hatching of eggs, while decreasing survival of coracidia (Hilliard, 1960). Plerocercoids of D. dendriticum within fish IH are more active and grow larger at warmer temperatures, probably causing more pathology in the fish (reviewed in Marcogliese, 2001). Thus, at warmer temperatures, there will be a trade-off between accelerated development of free-living stages and stages within poikilothermic IH, and decreased survival of both free-living coracidia and infected fish hosts ( Jenkins et al., 2011).

Synchronicity in the occurrence and availability of infective para-site stages and susceptible hosts is critical in the transmission dynamics of diphyllobothriids. Climate change is predicted to result in substantial mis-matches in timing of development for invertebrate prey (IH) and activity patterns for fish, mammals, and migratory avian hosts (Hoberg et al., in press). For example, transmission of D. dendriticum may be considerably dis-rupted due to asynchrony between temperature-driven hatching of cora-cidia and photoperiod-driven amplification of copepod populations, as well as asynchrony between the availability of copepods and a susceptible popu-lation of fish IH (Marcogliese, 2001). Shifts in seasonal timing (phenology) for migratory birds serving as definitive hosts may include early migration and nesting resulting in decreased food availability for breeding birds and fledglings (Marcogliese, 2001). This may drive shifts to alternative prey spe-cies (prey-switching), resulting in exposure to a broader spectrum of para-sites. Mismatches in the seasonal timing of these multiple production cycles are expected to disrupt patterns of parasite diversity. This may be reflected through loss of typical parasites, or declines in their abundance and preva-lence, and could also extend across migration corridors and staging areas.

Transmission of D. dendriticum to people also appears to be seasonally defined (in part due to freezing susceptibility of pleroceroids), with egg shed-ding in people peaking in late summer and fall (Curtis et al., 1988). As a con-sequence, climate change might extend the season of transmission, as fresh fish might be consumed by people (or fed to dogs) for a longer portion of the year. Finally, climate change might alter the location of traditional fishing grounds. If people transport fish for longer distances before processing, this could allow more time for migration of greater numbers of plerocercoids of D. dendriticum from the viscera to the musculature ( Jenkins et al., 2011).

In marine systems, environmental changes include variation in oceano-graphic structure, regime shifts (oscillations from warm to cold conditions), and range shifts for crustaceans, fish, and marine mammals. Directional cli-mate change interacts with long-term oceanographic-atmospheric regime shifts such as the Pacific Decadal Oscillation, and short-term variability,




particularly the North Atlantic Oscillation, which act as determinants of production cycles, trophic structure, and ecology of invertebrates, fish, sea-birds, and marine mammals in the Northern Hemisphere (Chavez et al., 2003; Hurrell et al., 2003). Collectively, these processes serve to determine the overall patterns of transmission, distribution, and abundance for diphyl-lobothriids circulating among marine mammals and seabirds (Hoberg, 2005; Hoberg and Adams, 2000; Hoberg et al., in press).

Decreases in sea ice in the Arctic basin are also predicted to have a perva-sive effect on ecosystem structure and the biology of ice-associated marine mammals, including walruses, seals, and whales that are primary hosts for marine diphyllobothriids (Moore and Huntington, 2008). Changes in oce-anic regimes, currents and water-mass structure, associated ice conditions, freshwater melt and salinity will drive modifications in behaviour and diets for marine mammals as distribution and species composition for inverte-brate and vertebrate prey species respond to new environmental conditions (Laidre et al., 2008; Marcogliese, 2001). The degree of sympatry and seasonal overlap in distributions for cetaceans and pinnipeds are predicted to increase, suggesting heightened opportunities for the exchange and dissemination of parasites such as diphyllobothriids (Burek et al., 2008).

10. ECHINOCOCCUS GRANULOSUS/CANADENSIS !CYSTIC HYDATID"

Echinococcus granulosus is a species complex of taeniid cestodes respon-sible for cystic hydatid disease in people worldwide. According to the World Health Organisation, hydatid disease is one of the most expensive parasitic zoonoses to treat and prevent world-wide (Eckert et al., 2001). Life cycles of E. granulosus involve carnivore DHs and herbivore IHs, and various species/strains utilise different assemblages of domestic livestock, wildlife, and people (Rausch, 1967). Adult cestodes, which are quite small (2–7 mm), reside in the small intestines of definitive hosts and shed eggs that are immediately infective for IHs. Ingested eggs release oncospheres that penetrate the intes-tinal wall of the new host, undergo tissue migration, and eventually create unilocular cysts containing larval protoscolices in organ tissue (most often the liver or lung). People are considered accidental hosts, in which cysts form but may not develop fertile protoscolices (Rausch, 2003).

10.1. Species and Strains Present in the NorthThere are at least 10 genotypes of the E. granulosus species complex that circulate in different host assemblages worldwide (Thompson et al., 2006).


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The pastoral strains (G1-3, E. granulosus sensu stricto), which circulate among domestic livestock and dogs, are not thought to be present in the North, although they have been introduced into sheep rearing regions of the west-ern continental USA (Rausch, 2003). In northern Canada, two genotypes (G8 and G10) circulate in largely sylvatic cycles involving cervids and wild canids (Fig. 2.21); only the G8 genotype has been reported in Alaska ( McManus et al., 2002; Thompson et al., 2006). It is possible that one or both of these genotypes may have been introduced into the North American Arctic along with infected reindeer imported from Siberia and Fennoscan-dia in the early part of the twentieth century (Rausch, 2003; Thompson et al., 2006); both G8 and G10 strains have been identified in Fennoscandia (Saarma et al., 2009).

The taxonomic status of the E. granulosus species complex is somewhat controversial. Initial phylogenetic analyses based on mitochondrial DNA suggested that the G6–G10 genotypes be unified as the species E. canadensis (Nakao et al., 2006; Thompson et al., 2006). However, more recent phylo-genetic analyses based on nuclear DNA suggest that only the G8 and G10

Figure 2.21 Life cycle of the cervid strain of Echinococcus granulosus (E. canadensis) in the North. The larval or metacestode stage takes the form of a unilocular hydatid cyst (cystic hydatid).




cervid strains be unified under the name E. canadensis, and the G6, G7, and G9 strains (in camels, pigs, and people, respectively) be unified as E. intermedius (Saarma et al., 2009). Therefore, in this review, E. canadensis will be used when referring to the cervid strain(s) present in North Amer-ica, differentiated into the G8 and G10 genotypes where relevant.

10.2. Geographic Distribution in the NorthEchinococcus canadensis is present across northern Canada and Alaska (Fig. 2.22) but is not established in Greenland (Rausch, 2003). In Canada, E. canadensis is present in all provinces and territories with the exception of the East Coast (provinces of Nova Scotia, Prince Edward Island, New Brunswick and the island of Newfoundland) where wolves (C. lupus) have been historically absent (Sweatman, 1952). Indeed, E. canadensis remains common in the North wherever wolves and ungulates co-exist (44–68°N); however, it may be absent in the High Arctic islands due to the low year-round density of ungulate IHs ( Jenkins et al., 2011; Miller, 1953; Sweatman, 1952). E. canadensis is not present on the island of Newfoundland due to

Figure 2.22 Published reports of cystic hydatid disease (Echinococcus canadensis) in ungulates in the North. (Animal data from Table 2.16). Clinical cases have been documented in people (Table 2.17), and serological surveys are reported in Table 2.18.


Arctic Zoonoses 147


the extirpation of wolves in the early part of the twentieth century, even though ungulate IHs (moose, A. alces, and caribou, Rangifer tarandus) are abundant. However, recent colonisation by coyotes (C. latrans) may enable local transmission of E. canadensis.

10.3. Transmission, Prevalence, and Animal Health Impact in the NorthThe sylvatic strains of E. canadensis cycle primarily between canid definitive hosts and cervid IH via sympatric predator–prey relationships. In northern Canada and Alaska, the larval cysts are detected most commonly in moose and caribou/reindeer (Table 2.16); however, other ungulate IH have been reported, including wapiti (Cervus canadensis) OMIT (C. elaphus), muskoxen (O. moschatus), mountain goats (Oreamnos americanus), American bison (Bison bison) and black-tailed deer (Odocoileus hemionus) (Cameron, 1960; Cho-quette et al., 1957; Hadwen, 1932; Rausch and Williamson, 1959; Sweat-man and Williams, 1963; Thomas, 1996). Earlier reports of hydatid cysts in microtine rodents are most likely to be Echinococcus multilocularis (Rausch and Schiller, 1951); grey squirrels (Sciurus carolinensis) have been experi-mentally infected with E. granulosus (Sweatman and Williams, 1963). Adult cestodes have been reported in the intestinal contents of wolves, coyotes, and domestic dogs (C. lupus familiaris) (Choquette and Moynihan, 1964; Jenkins et al., 2011; Jones and Pybus, 2001; Miller, 1953; Rausch and Williamson, 1959; Sweatman, 1952). According to Rausch (1956b), historical reports of E. granulosus in red fox (V. vulpes) and arctic fox (V. lagopus) in Alaska and the Northwest Territories were more likely to be E. multilocularis. Foxes are no longer considered to be natural hosts of E. granulosus/canadensis (Rausch 1956b).

In sub-Arctic and Arctic regions of North America, the prevalence of infected animals is highly variable among different host species and between locations, and comparisons are difficult due to a range in detection effort and methods. In IH, moose in northern Alaska were reported to have a higher prevalence of infection than those in the south (24% and 4%, respectively), and 0.5–6% of caribou were infected (Rausch, 1952, 1959b; Rausch and Williamson, 1959) (Table 2.16). Between 3% and 5% of Alaskan reindeer were reported infected with E. canadensis (Rausch, 2003; Sweatman and Williams, 1963). In Canada, moose in the Yukon Territories were infected at high prevalence (43%), as were caribou/reindeer in the Northwest Territories (20–35%). In sub-Arctic and temperate regions of Canada, wapiti were infected at a somewhat lower prevalence (6–21%) (Sweatman and Williams, 1963).



148


Table 2.16 Prevalence [% (n)] of Hydatid Cysts of Echinococcus canadensis as Determined Through Necropsy of Ungulates (Order Artiodactyla) in Alaska and Northern Canada (from west to east, then chronologically within a host species)Host Location Prevalence [% (n)] References

Black-tailed Deer (Odocoileus hemionus columbianus)

Baranof Island, AK 1 case Rausch and Williamson (1959)

Caribou (Rangifer tarandus) Central Brooks Range, AK <1 (200) Rausch (1952)Nelchina, AK 6 (67) Skoog in Rausch and

Williamson (1959)Central Brooks Range, AK 3 (79) Rausch (2003)NR, AK 5 (63) Rausch (2003)Northern SK and Wholdaia Lake,

NT21 (14) Harper et al. (1955)

Aklavik, NT 905 (1664) Choquette et al. (1957)Fort Smith, NT 35 (17) Sweatman and Williams (1963)Reindeer Station, NT 20 (517) Sweatman and Williams (1963)Fort Smith, NT 3.9 (1258) Thomas (1996)George River, NL 1.3 (159) Parker (1981)

Moose (Alces alces) Railbelt-Matanuska Valley, AK 24 (101) Rausch (1959b)Anchorage,-Upper Kenai, AK 4 (23) Rausch (1959b)Dawson City, YT 43 (154) Sweatman and Williams (1963)Le Pas, MB 1 case Hadwen (1932)

Mountain Goat (Oreamnos americanus) Lynn Canal, AK 1 case Rausch and Williamson (1959)Muskoxen (Ovibos moschatus) Thelon Game Sanctuary, NT 3 (3) Gibbs and Tener (1958)

Ellesmere Island, NU NR Tener, 1965 in Marquard-Petersen (1997)

Abbreviations for states, provinces, and territories as in Fig. 2.1.NR – not recorded.


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Sporadic cases in ungulates in northern regions of Saskatchewan, Manitoba, and Labrador have also been reported (Hadwen, 1932; Harper et al., 1955; Parker, 1981).

Detection of Echinococcus spp. infection in definitive hosts has historically relied on collection of adult cestodes from the intestines during necropsy. Identification of Echinococcus eggs detected in faeces is complex as eggs are indistinguishable from other taeniid species; therefore, molecular meth-ods are required for identification, which have only recently been applied in North America. Using these methods, 6% of faecal samples from free-ranging dogs in one community in the northern SK contained eggs of E. canadensis (G10) (Himsworth et al., 2010a), but in other communities, only eggs of Taenia spp. were detected (Schurer et al., 2012). Several Taenia spp. have distributions in wild canids that overlap E. granulosus in the North, including T. crassiceps, T. pisiformis, and T. polyacantha ( Jones and Pybus, 2001). Taeniid eggs were detected in 5% of 423 wolves in Greenland, but were not identified further (Marquard-Petersen, 1997).

In Alaska, based on recovery of adult cestodes at necropsy, 30% of 200 wolves were infected with adult cestodes of Echinococcus spp., with sled dogs (10–22%) also reported as common hosts (Rausch, 1952, 2003; Rausch and Williamson, 1959). A similar prevalence (also based on necropsy) is reported in wolves in the Yukon Territory (22%; N = 89) as well as in the Northwest Territories (24%; N = 21) (Choquette et al., 1973). One survey of dogs culled from eight towns in Northwest Territories reported a 12% preva-lence (4/33) of E. granulosus/canadensis (Miller, 1953).

The overall impact of E. canadensis infection on IHs is unknown, but varies according to parasite load, cyst location, and host species. In moose IHs, hydatid cysts (metacestodes) are present in various organs (the lung, liver, spleen, heart, and kidneys), while in wild reindeer, cysts are generally restricted to the lungs (Addison et al., 1979; Rausch, 2003). High intensity of hydatid cysts in moose are thought to increase the likelihood of preda-tion by wolves or human hunters, possibly due to decreased stamina and pulmonary function as a result of space-occupying lung lesions ( Joly and Messier, 2004; Rau and Caron, 1979). Infected canid definitive hosts do not appear to be at risk of increased morbidity or mortality, and generally experience no adverse effects.

Treatment and control programmes for E. granulosus/canadensis focus on the regular administration of cestocidal drugs for definitive hosts, and on good hygiene practices. The latter includes preventing dogs from ingesting the viscera of infected IHs and ensuring proper disposal of canine faeces.




Praziquantel is the only drug currently labelled to remove adult cestodes of E. granulosus from domestic dogs; however, nictroscanate has also proven effective when administered at double the dose recommended for other parasites (Ramsey, 2011). Veterinary practitioners in Canada and Alaska would be unlikely to attempt treatment of the metacestode stage in cap-tive cervids, as diagnosis is cost prohibitive and technologically challenging. However, benzimidazoles such as albendazole and oxfendazole have effec-tively inactivated protoscolices in IH (Blanton et al., 1998).

10.4. Transmission, Prevalence, and Public Health Impact in the NorthPeople are exposed to E. canadensis through the accidental ingestion of eggs passed in the faeces of definitive hosts (wolves, coyotes, and dogs). These eggs are immediately infective once they have passed into the environment, and may adhere to the coat of an animal and a wide variety of surfaces (Laws, 1968). Theoretically, hunters and trappers of wild carnivores could be at risk due to their close contact with carnivore hides, faeces and intestines, as well as dog owners who reside in endemic areas. Although the relative significance of these exposure routes is currently unknown, it is likely that people are predominantly infected though ingestion of contaminated sur-face water, produce, and soil. The eggs of Echinococcus spp. and related tae-niids are extremely resistant to extremes of temperature and humidity and can persist in the environment for several years (Colli and Williams, 1972; Eckert et al., 2001). Domestic or free-roaming dogs are considered impor-tant ‘bridging hosts’ between people and wildlife due to their nonselective diet and their close contact with people (Rausch, 2003). Subsistence hunt-ing within a community, where dogs have access to offal and carcasses, is also considered an important risk factor for human exposure to E. canadensis (Himsworth et al., 2010a). However, people are not infected through con-sumption of meat or organs from wild game but instead through contact with faeces of dogs that have scavenged carcasses or been fed offal.

Cystic hydatid disease in people is most often characterised by unilocu-lar fluid-filled cysts in the liver and lungs, although aberrant locations such as the brain have also been documented (Himsworth et al., 2010a; Somily et al., 2005; Wolfgang and Poole, 1956). Symptoms can include coughing, anorexia, fever, shortness of breath, chest, or abdominal pain, and functional neurological deficits if cysts are associated with the brain, nerves, or spi-nal cord (Moore et al., 1994; Somily et al., 2005). Echinococcus canadensis (or the cervid G8/G10 strains of the E. granulosus species complex) has been


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considered to be less likely to cause anaphylactic shock and secondary seed-ing than the pastoral strain(s) (G1–G3) (Castrodale et al., 2002). Autochtho-nous cases of cystic hydatid disease in Canada and Alaska do not commonly result in fatality; however, infection with the G8 strain has been known to cause severe clinical disease, and most recently, death (Castrodale et al., 2002; McManus et al., 2002). Treatment options for hydatid disease include surgical removal, benzimidazole chemotherapy, and puncture–aspiration–injection–reaspiration therapy (Brunetti et al., 2010). In ideal circumstances a physician might use a ‘watch-and-wait’ strategy to monitor and treat this disease; however, the limited availability of medical imaging equipment and geographic barriers to accessing medical care may make this approach impractical in northern communities (Brunetti et al., 2010; Lamy et al., 1993; Pinch and Wilson, 1973).

Human cystic hydatid disease did not appear in Canadian literature until 1883, and until the 1950s (Table 2.17), most cases were detected in immigrants from Iceland, an area historically endemic for the pastoral vari-ant of E. granulosus (Cameron, 1960). In Alaska, the first human case was recorded in 1941 (Rausch, 1968; Wilson et al., 1968). Human hydatid dis-ease is reportable to Alaskan state public health authorities; peak numbers of cases were detected from 1953 to 1973 (Fig. 2.23), nearly all of which were Indigenous people (Rausch, 2003). Cases of autochthonous hydatid infection were reported with increasing frequency in Canadian Indigenous populations in the latter half of the twentieth century, mainly due to inci-dental observation of cysts during tuberculosis screening (Lamy et al., 1993). Similar to Alaska, 99% of 141 cystic hydatid cases in Canada in the 1950s occurred in Indigenous people (Miller, 1953).

In 1952, Indian Health Services and the Institute of Parasitology in Can-ada initiated efforts to determine the prevalence of infection in Indigenous communities using the Casoni skin test. Initial efforts used antigen obtained from Australian sheep cysts that was soon replaced by antigen obtained from reindeer in Aklavik (YT), resulting in greater test sensitivity (Cameron, 1960; Wolfgang and Poole, 1956). Between 1954 and 1957, positive Casoni skin test results were found in 6–52% of people across northern Canada (N = 3429) (Table 2.18). This proportion was lower in Alaska where the skin test employed did not use antigens of E. canadensis (Davis, 1957). Cul-tural practices including food preparation, acquisition of locally acquired foods, outdoor food storage, and the presence of large working dog popula-tions may have significantly increased the risk of hydatid infection in the middle of the twentieth century.



152


Table 2.17 Cases of Cystic Hydatid Disease in People in Alaska and Canada, Organised ChronologicallyLocation Sampling Dates Number of cases Reference

Alaska, USA

1941 1 Magath in Wilson et al. (1968)1948 1 Williams in Wilson et al. (1968)1949–1960 41 Rausch (1960)1950–1966 101 Wilson et al. (1968)1966–1973 25 Pinch and Wilson (1973)1950–1990 >300* Castrodale (2003)1991–2003 8 Castrodale (2003)1999 2 Castrodale et al. (2002)

Canada

Central Canada Prior to 1883 8–10 Osler in Cameron (1960)Northwestern Canada 1948–1955 At least 180 Miller (1953); Choquette and

Moynihan (1964)ON 1967–1982 40 Langer et al. (1984)NT and Northern AB 1970–1992 14 Moore et al. (1994)Southern BC 1987–1991 5 Finlay and Speert (1992)MB and ON 1987–1997 17 Al Saghier et al. (2001)Northwestern Canada 1991–1993 3 Lamy et al. (1993)NT, Northern AB 1991–2001 22 (+20 possible) Somily et al. (2005)Canada 2001–2005 108 cases Gilbert et al. (2010)SK 2008 1 Himsworth et al. (2010a)

Note that Alaskan cases are also captured in Fig. 2.23. Abbreviations for states, provinces, and territories as in Fig. 2.1.*Includes the previous three citations.


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Today, imported and authochthonous cases of cystic hydatid disease occur infrequently in North America, in part due to the eradication of E. granulosus in Iceland, global efforts to control the disease, and the grad-ual phasing out of sled dogs as a method of transportation in the North. In Alaska, where human cases are reportable, zero to three cases per year in Indigenous and other residents have been reported since 1973 (Fig. 2.23). In Canada, neither human nor animal cases are nationally reportable (although laboratory confirmed cases in animals are annually notifiable to the World Organisation for Animal Health), so surveillance is limited to case reviews and serosurveillance.

A review of records in Edmonton hospitals, which act as referral cen-tres for northern Alberta and the Northwest Territories, identified 42 cases of suspected or confirmed cystic hydatid disease between 1991 and 2001 (Somily et al., 2005). Indigenous patients were over-represented in this group, as 41% self-identified as Indigenous, compared with the 5% of Alber-tans and 3% of Canadians who self-identified as Indigenous in 2001. These results are supported by Gilbert et al. (2010), who reviewed hospital cases

Figure 2.23 Cases of cystic hydatid disease in people in Alaska, 1940–2010, as reported to the state public health authorities.



154


Table 2.18 Prevalence [% (n)] of Exposure to Echinococcus granulosus/canadensis in People Residing in Alaska and Northern CanadaLocation Sampling Dates Prevalence [% (n)] Method References

Alaska, USA

Fort Yukon 1957 16 (104) ST* Davis (1957)Beaver, Tanana Stevens Village 1957 21 (168) ST† Tulloch in Davis (1957)

Canada

YK 1954 38 (293) ST‡ Wolfgang and Poole (1956)Mackenzie Delta to Great Slave Lake, NT 1955 41.5 (1145) ST‡ Wolfgang and Poole (1956)Great Slave Lake, NT 1955 13.5 (584) ST‡ Wolfgang and Poole (1956)Inuvialuit Settlement Region, NT 2007–2008 <1 (362) SE** Egeland et al. (2010a)Northeastern SK 2008 11 (106) SE Himsworth et al. (2010a)Keewatin Yatthe Region, SK 2011 48 (201) SE Schurer et al. (2013)Arviat, NU 1956–1957 52 (186) ST‡ Whitten in Cameron (1960)Igoolik, NU 1956–1957 6 (63) ST‡ Whitten in Cameron (1960)

Quebec

Nunavik, QC 1980s <1 (759) SE Tanner et al. (1987)Nunavik, QC 2004 8.3 (917) SE Messier et al. (2012)James Bay, QC 1980s <1 (436) SE Tanner et al. (1987)James Bay, Eastmain and Wemindji, QC 2007 4 (250) SE Campagna et al. (2011)James Bay, Chisasibi and Waskaganish, QC 2008 <1 (266) SE Sampasa-Kanyinga et al. (2012)Nunatsiavut Health Survey, NL 2007–2008 <1 (310) SE Egeland et al. (2010b)

*Skin test = ST – with antigen acquired in New Zealand.†Lilly skin test.‡Casoni skin test with reindeer antigen.**Serology.


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using ICD codes for Echinococcus/hydatid disease across Canada between 2001 and 2005 (N = 108). In this review, people living north of the 55th parallel were 4.88 times (95% CI 2.52–9.44) more likely to be hospitalised for cystic hydatid disease than the average Canadian (2.9 cases versus 0.72 cases per 1,000,000 people annually). Hospital records also indicate that women may be at higher risk of developing hydatid disease than men (RR 1.92, 95% CI 1.29–2.87)(Gilbert et al., 2010; Langer et al., 1984; Somily et al., 2005).

Casoni skin tests have been replaced with serological testing in the northern and Indigenous communities based on IgG ELISA (Tanner et al., 1987). Seroprevalence in Inuit and James Bay Cree, QC (0.1–4%) and First Nations in Saskatchewan (11% and 48%) indicate that northern and Indig-enous populations, especially in western Canada, continue to be at risk for exposure to E. canadensis. However, the association between positive serology and clinical cystic hydatid disease is unclear. As well, this disease is underdiagnosed due to a variety of factors including many asymptomatic cases, nonspecific symptoms, the long progression of the disease, and a wan-ing awareness in the medical community. Therefore, these factors should be considered when interpreting the apparent decline in prevalence of cystic hydatid disease in human populations in North America.

10.5. Future Impact of Climate and Landscape ChangeThe worldwide distribution of strains in the E. granulosus species complex demonstrates that this group of cestodes transmits well in different climates and in a wide variety of hosts (Mas-Coma et al., 2008); however, species and genotypes may vary in hardiness (Eckert et al., 2001; Jenkins et al., 2011). Echinococcus canadensis is particularly well adapted to cold northern climates. Eggs that passed in the faeces of definitive hosts can survive in the envi-ronment for several years before infecting a new host; eggs and cysts may survive even longer if encased within a protective barrier (e.g. snow, faeces, sewage, or a host carcass) (Eckert et al., 2001). Temperatures above +35 °C or below "30 °C can damage eggs, while temperatures above 60 °C or below "70 °C completely inactivate them (Colli and Williams, 1972; Gem-mell, 1973; Mas-Coma et al., 2008). Regardless of temperature, Echinococcus eggs are sensitive to desiccation at low humidity and are inactivated within one day at 0% relative humidity (RH) and within four days at 25% RH (Eckert et al., 2001; Gemmell 1973). Diker et al. (2007) tested the viability of hydatid cysts from sheep (E. granulosus) at a variety of temperature and RH combinations in the laboratory, and estimated environmental survival




times for cysts in discarded carcasses: 3–36 days in winter ("10 to 0 °C), 12–28 days in spring/autumn (10–20 °C), and 3–4 days in summer (30–40 °C) (Diker et al., 2007). This has limited application to the North, where winter air temperatures drop far below "10 °C and the species present is E. canadensis. Egg and cyst viability experiments demonstrate that the duration of cold and freeze–thaw cycles are more important to inactiva-tion than the magnitude of cold (Davis, 1957).

Density increases in moose populations are associated with increasingly aggregated distributions and increases in prevalence of E. canadensis ( Joly and Messier, 2004). The northern distribution of moose in Canada and Alaska is thought to be limited by snow cover and vegetation; however, warming trends that increase food availability could allow moose to move further north (Darimont, 2005). Woodland and barren-ground caribou populations are currently decreasing as a result of anthropogenic and natural environmental changes, but could potentially be replaced by other ungu-late hosts suitable for harbouring E. canadensis, such as moose and wapiti (McLoughlin et al., 2002; Vors and Boyce, 2009). If the snow cover decreases by 10–20%, as predicted, the High Arctic could become more supportive of densely populated predator–prey food webs and might become a new area for emergence of E. canadensis (Davidson et al., 2011).

Arctic temperatures over the last 2000 years were warmest in the period between 1950 and 2000, despite a previous cooling period (Kaufman et al., 2009). Mean annual precipitation in the Canadian Arctic has increased by 2–25% over the last 62 years (Furgal and Prowse, 2008). With regard to effects on transmission of E. canadensis in the future, novel weather patterns may alter sympatric territories of predator–prey systems or egg survival in the environment, possibly resulting in the emergence of hydatid disease into new areas, as well as retreat from warming areas (eggs have decreased sur-vival in warmer temperatures). Warming winter temperatures could increase the window of opportunity for hydatid cysts (which are freeze susceptible) to survive before infecting a new definitive host. Increased precipitation in the north is protective for eggs against desiccation, but could also limit the accessibility of eggs on vegetation for ingestion by IHs ( Jenkins et al., 2011). Climate change could cause breakdowns in sanitation infrastructure, potentially reducing access to clean water through events such as water contamination with eggs of Echinococcus (Parkinson and Evengard, 2009; Schwabe, 1984). Finally, emergence of a related species (E. multilocularis) as a result of increased globalisation, climate and landscape change, and altered interfaces with wildlife reservoirs serves as an important reminder about the


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versatility of these cestodes (Davidson et al., 2012; Jenkins et al., 2011; Mas-Coma et al., 2008; Schweiger et al., 2007).

11. ECHINOCOCCUS MULTILOCULARIS !ALVEOLAR HYDATID"

Echinococcus multilocularis is a taeniid cestode responsible for alveolar hydatid disease (also known as alveolar echinococcosis or alveolar hydatido-sis) in people around the circumpolar North. Adults of this cestode are pres-ent in the small intestine of wild carnivores, such as foxes, domestic canids, and felids (Fig. 2.24). Eggs passed in the faeces are immediately infective for rodent IHs. Ingested eggs release oncospheres that penetrate the intestinal wall of the IH, undergo tissue migration, and eventually develop into alveo-lar (=multilocular) hydatid cysts, which generally originate in the liver and can fill the entire abdominal cavity. The life cycle is complete when a car-nivore consumes the alveolar hydatid cyst in the rodent, whereupon proto-scolices evert, attach to the intestinal wall, and begin to produce proglottids. People and other mammals can serve as aberrant IHs, in which protoscolices may not develop and the germinal membrane metastasises throughout the liver and other organs.

Figure 2.24 Life cycle of Echinococcus multilocularis in the North. The larval or meta-cestode stage takes the form of a multilocular hydatid cyst (alveolar hydatid).




11.1. Species and Strains Present in the NorthConfusion over the identity and biological relationship of E. granulosus and E. multilocularis was only resolved in the past 60 years (Tappe et al., 2010). Resolution of a long and ongoing controversy about the biology of these species only emerged following recognition and clarification of the taxonomy for what we now regard as E. multilocularis in Alaska (Rausch and Schiller, 1954). Up to that time, considerable contention existed as to whether or not the distinct zoonoses attributable to these taeniids were caused by variants of a single species. Final clarification of this significant question emerged from the field and laboratory studies conducted in Alaska by Robert Rausch and Everett Schiller, who were the first to unequivocally complete the cycle for E. multilocularis from arvicoline IHs through arc-tic fox definitive hosts (Rausch and Schiller, 1951). Although Rausch and Schiller (1954) initially regard the forms found on St. Lawrence Island as a distinct species, Echinococcus sibiricensis, it was later shown that these popula-tions were conspecific with E. multilocularis, thus establishing a Holarctic range for this parasite. Further, alveolar hydatid disease was documented in the indigenous population of St. Lawrence Island, representing the first rec-ognised cases for E. multilocularis as a zoonotic pathogen in North America.

Recent findings that E. multilocularis is not genetically uniform across its distribution in the northern hemisphere have significance for understanding pathogenicity, host specificity, and zoonotic potential (Knapp et al., 2009; Nakao et al., 2009). Characterisation at multiple mitochondrial loci has demonstrated distinct North America, Asian, and European haplotypes of E. multilocularis (Nakao et al., 2009). On St. Lawrence Island, Alaska, there are three known strains of E. multilocularis, a North American N1 haplotype and two Asian strains, A2 and A4 (Nakao et al., 2009). The presence of two Asian haplotypes in Alaska are likely due to the natural movement of arctic foxes (Vulpes, formerly Alopex, lagopus), which travel extensive distances across the ice (Dalen et al., 2005; Fay and Williamson, 1962; Hoberg et al., 2012). This dispersal could lead to the eventual introduction of additional European or Asian strains of E. multilocularis to North America and Greenland.

A second North American haplotype of E. multilocularis (N2), which is distinct from those present on St Lawrence Island, Alaska, has been described in the north central region (NCR) of North America (Nakao et al., 2009). The NCR of North America corresponds to the southern portion of the three Canadian prairie-provinces and contiguous American states. It is unlikely that the N2 strain is present in the Arctic due to the lack of sup-portive vegetation in the boreal region, which has created an area of low


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rodent IH density, resulting in separate northern and southern populations of E. multilocularis in North America (Nakao et al., 2009; Schantz et al., 1995).

11.2. Geographic Distribution in the NorthThere are two distinct populations of E. multilocularis in North America. The northern population is found in the Arctic tundra region of Canada and Alaska, and the second population is found in the North American NCR (Eckert et al., 2001; Jenkins et al., 2011; Nakao et al., 2009). The southern distributional limit of E. multilocularis in the Canadian Arctic is thought to roughly follow the southern distribution of arctic foxes, which in turn, roughly follows the northern border of the tree line. Actual reports of this parasite in Arctic Canada are limited to one report on the mainland and two in the high Arctic (Fig. 2.25). In Alaska, the distribution of E. multilocularis is also thought to correspond to the distribution of the arctic fox and appears to be largely limited to coastal regions of the northern Alaskan mainland

Figure 2.25 Published reports of alveolar hydatid disease (Echinococcus multilocularis) in the North based on necropsy in animals (foxes, dogs, and rodents) and immunologi-cal and clinical testing of people. (Data from Tables 2.19 and 2.20). Human cases have not been described in northern Canada and the parasite is not thought to be present in Green-land.




and the Alaskan Archipelagos (Fay and Williamson, 1962) (Fig. 2.25). Red fox (V. vulpes) is also a suitable definitive host, whose distribution is now sympatric with arctic fox in many regions of the Arctic mainland (Her-steinsson and MacDonald, 1992; Rausch, 1956b). Although arctic foxes are present in Greenland, to date, E. multilocularis has not been reported in any hosts in Greenland (Braestrup, 1941; Kapel and Nansen, 1996).

11.3. Transmission, Prevalence, and Animal Health Impact in the NorthDefinitive hosts for E. multilocularis in the North American Arctic include canid species such as arctic fox, red fox, and domestic dogs (C. lupus familia-ris) (Table 2.19). Wolves (C. lupus) may also serve as definitive hosts but are more likely to be infected with E. granulosus (Rausch, 2003). Although the domestic cat (Felis catus) and lynx (L. canadensis) may also serve as definitive hosts for E. multilocularis, felids in general appear to be less suitable definitive hosts (Kapel et al., 2006). In addition, lynx are not well-established north of the boreal forest and free-ranging domestic cats are uncommon in northern communities. Intermediate hosts in the North include arvicoline rodents (lemmings, voles, and muskrats) and neotomine rodents (such as deer mice) ( Jones and Pybus, 2001). Other rodents, such as ground squirrels (Family Sciuridae) and shrews (Family Soricidae), have been reported in a highly endemic focus on St Lawrence Island (Table 2.19). In Greenland, the only potential IH is the Greenland (collared) lemming (Dicrostonyx groenlandicus). However, field and laboratory studies indicate that the collared lemming, despite being a close relation to the brown lemming (Lemmus trimucronatus), is not a suitable host for E. multilocularis (Ohbayashi et al., 1971; Rausch, 1995).

The prevalence of E. multilocularis in both definitive hosts and interme-diate hosts on the Canadian Arctic islands and in the mainland North American Arctic is relatively low. Surveys on the Arctic mainland have found the prevalence of E. multilocularis in red and arctic foxes to be only 2–9% (Table 2.19). In studies of rodent IHs on the mainland of Alaska, E. multilocu-laris has not been found in excess of 1% despite multiple surveys (Holt et al., 2005). Rausch (1956b) reported examining 2500 rodents, which he consid-ered a ‘relatively small’ number, with no observed cysts. To our knowledge, IH surveys have not been performed in the Canadian Arctic.

In contrast, St. Lawrence Island in the Bering Strait, as well as St. George and Nunivak Islands in the Bering Sea, are considered hyperendemic foci of transmission of E. multilocularis, with prevalence ranging from 32 to 100% in arctic fox and 5–13% in dogs (Table 2.19). The discrepancy between


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Table 2.19 Prevalence [% (n)] of Echinococcus multilocularis Identi!ed at Necropsy of Carnivore De!nitive Hosts and Rodent/Shrew IH in Alaska and Northern CanadaHost Location(s) Prevalence [% (n)] References

Order Carnivora

Arctic Fox (Vulpes lagopus) St. Lawrence Island, AK 71 (7) Rausch and Schiller (1951)67 (6) Thomas et al. (1954)40 (106) Rausch and Schiller (1956)100 (40) Rausch and Schiller (1956)75 (1527) Rausch (1967)80 (1579) Rausch and Fay (2002)

St. George Island, AK 67 (5) Fay and Williamson (1962)32 (28) Rausch (1967)

Nunivak Island, AK 73 (33) Rausch (1967)Seward Peninsula, AK 2 (11) Rausch (1967)Mainland, AK 4 (94) Rausch (1956b)Mainland, AK 9 (207) Rausch (1967)Banks Island, NT 2 (50) Eaton and Secord (1979)Eskimo Point (Arviat), Resolute

Bay, Cornwallis Island, NUNR Choquette et al. (1962)

Dog (Canis lupus familiaris) St. Lawrence Island, AK 6 (89) Rausch (1960)5 (110) Rausch (1967)13 (31) Rausch and Fay (2002)

Red Fox (Vulpes vulpes) Nunivak Island and Point Barrow, AK

2 (100) Rausch (1956b)

Nunivak Island and Brooks Range, AK

55 (11) Rausch (1967)

Continued



162


Host Location(s) Prevalence [% (n)] References

Order Rodentia

Brown Lemming (Lemmus trimucronatus)

Mainland Alaska <1 (467) Holt et al. (2005)

Ground Squirrel (Citellus undulatus)

St Lawrence Island, AK 17 (12) Thomas et al. (1954)

Red-back Vole (Clethrionymus rutilus)

St Lawrence Island, AK 18 (22) Rausch and Schiller (1956)

12 (25) Rausch and Schiller (1956)5 (22) Rausch and Schiller (1956)

Tundra Vole (Microtus oeconomus) St Lawrence Island, AK 2 (385) Rausch and Schiller (1951)8 (905) Rausch and Schiller (1956)16 (200) Rausch and Schiller (1956)10 (320) Rausch and Schiller (1956)5 (528) Rausch et al. (1990a)28 (1115) Rausch et al. (1990b)63 (329) Rausch and Fay (2002)

Voles St Lawrence Island, AK 17 (198) Thomas et al. (1954)

Order Soricomorpha

Shrew (Sorex jacksoni) St Lawrence Island, AK 25 (4) Thomas et al. (1954)23 (13) Rausch and Schiller (1956)

Abbreviations for states, provinces, and territories as in Fig. 2.1.NR – Not recorded.

Table 2.19 Prevalence [% (n)] of Echinococcus multilocularis Identi!ed at Necropsy of Carnivore De!nitive Hosts and Rodent/Shrew IH in Alaska and Northern Canada—cont’d


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the mainland- and island infection rates may be due to the differences in rodent population stability. The island host populations tend to remain relatively stable from year to year while rodent populations on mainland Alaska experience dramatic fluctuations (Rausch and Fay, 2002). In years when infections in definitive hosts on St. Lawrence Island were between 76 and 100%, the prevalence of infection in rodent IHs did not exceed 20% (Rausch, 1956b). Although the published literature shows a range of 2–63% prevalence in rodents (primarily voles and shrews) on St. Lawrence Island (Table 2.19), the prevalence of infection in rodents on the island has at times exceeded 80% (Rausch et al., 1990a). Variation in infection rates among definitive and intermediate host species serve to highlight the role that definitive hosts play in parasite bioaccumulation. In fact, Fay and Wil-liamson (1962) noted that an infection rate of less than 10% in tundra voles (Microtus oeconomus) could yield almost 100% infection rates in Arctic foxes.

Prior to the implementation of an Echinococcus control programme, the rate of infection on St. Lawrence Island was approximately 53% in voles (Rausch et al., 1990b). The control programme, consisting of monthly doses of praziquantel for local dogs near Savoonga, decreased the occurrence of this parasite in voles by approximately 83% (Rausch et al., 1990b). These control measures remain the recommended approach to controlling E. mul-tilocularis in synanthropic cycles involving dogs (and cats) with access to infected rodent IHs; praziquantel has good efficacy against adult cestodes (Eckert and Deplazes, 2004; Eckert et al., 2001). Other recommended prac-tices in endemic regions include dog population control, community efforts to control free-roaming dogs, ‘poop scooping’, and thorough hand washing following handling of dogs, trapped or hunted foxes and coyotes, and their faeces. At the consumer/food handler level, thorough washing of fruits and vegetables harvested in regions where this parasite is present, and effective filtering of untreated surface water prior to consumption, are recommended.

Motivation for control programmes largely stems from public health significance. Rarely, E. multilocularis can cause alveolar hydatid cysts in dogs, resulting in severe disease similar to that observed in people (Eckert and Deplazes, 2004). Treatment is similar to that recommended in peo-ple with alveolar hydatid disease, involving an aggressive surgical removal and long-term parasitostatic treatment with benzimidazoles (Peregrine et al., 2012). Control in sylvatic cycles is more challenging than in synan-thropic cycles. To reduce human risk of exposure, wildlife population con-trol measures and good garbage management practices are recommended in urban areas in endemic regions. In lieu of mass culling, regular doses




of praziquantel-containing baits for wild carnivores in endemic regions may decrease the bioaccumulation of eggs in the environment (Eckert and Deplazes, 2004; Eckert et al., 2001).

11.4. Transmission, Prevalence, and Public Health Impact in the NorthPeople may become infected with E. multilocularis by the accidental ingestion of eggs shed in carnivore faeces. The sticky eggs may adhere to multiple sur-faces in the environment including vegetation, fur and human skin and may even float in water (Hildreth et al., 2000; Laws, 1968). In people, alveolar hyda-tid disease behaves like an invasive neoplasm, most often originating in the liver, with a case fatality rate that exceeds 90% within 10 years unless treated early and aggressively (Kern et al., 2003). While detection of cysts smaller than 10 mm is difficult, early detection and surgical resection of the infected tissue is essential to survival (Eckert et al., 2001; Rausch and Wilson, 1985). In North America, cases of human alveolar hydatid disease have occurred mainly in Alaska, with only two cases in central North America (Minnesota, USA and Manitoba, Canada) (Gamble et al., 1979; James and Boyd, 1937). Autochthonous cases of human alveolar hydatid disease have been primarily focused in the Alaskan Archipelagos with a few additional cases on the North Slope of the Alaskan mainland (Wilson et al., 1995) (Table 2.20).

Since the 1950s, 54 human cases of alveolar hydatid disease have been reported between 1947 and 1986 in Alaska (Castrodale, 2003) (Fig. 2.26). Historically, the transition of the Inupiat Inuit to a sedentary way of life negated the sanitary effects of a previously nomadic lifestyle, increasing the rate of human infection (Rausch, 2003). Domestic dogs, replacing Arctic fox as definitive hosts in villages, had access to stable and abundant populations of infected IHs, which served to perpetuate the life cycle of E. multilocu-laris and increase its prevalence in the immediate surroundings (Eckert and Deplazes, 2004; Stehr-Green et al., 1988). Domestic dogs are considered the most important source of transmission of this parasite to people primarily due to close physical proximity (Rausch, 1956b; Wilson et al., 1995). Trap-pers and hunters may also be at increased risk when handling infected foxes, although trapping foxes was not a significant risk factor in adults in a case-control study in Alaskan Eskimo (Rausch, 1956b; Stehr-Green et al., 1988). Around the world, the highest incidence of human infections with alveolar hydatid disease are primarily seen in rural areas where exposure is thought to occur through the accidental ingestion of eggs on local produce and vegetation (Hildreth et al., 2000). In some regions, consumption of surface


Arctic Zoonoses 165


(vs. well) water is associated with increased risk of alveolar hydatid disease (Yang et al., 2006).

At its peak, seropositivity for alveolar hydatid disease on St. Lawrence Island reached 98/100,000 (Schantz et al., 1995; Wilson and Rausch, 1980). However, there are significant challenges in the sensitivity and specificity of immunological testing for exposure to E. multilocularis, including the pos-sibility of cross-reaction with E. granulosus and related helminths. Therefore, ultrasound examination of the liver is considered the method of choice for detection of E. multilocularis infection in people, complemented by com-puted tomography or medical imaging in some cases (Eckert and Deplazes, 2004; Eckert et al., 2001). The historical presence of E. multilocularis in both human and animal hosts on the mainland of Alaska has been comparatively low (Rausch and Fay, 2002). Since the successful implementation of educa-tion and control programmes in 1986, there have been no reports of human E. multilocularis infection in Alaska (Castrodale, 2003) (Fig. 2.26). There is, however, the possibility of undiagnosed cases within Alaska and in other Arc-tic regions, as alveolar hydatid disease can mimic other conditions, including

Figure 2.26 Cases of alveolar hydatid disease (E. multilocularis) reported in people in Alaska, 1940–2010. The last case was reported in 1986.




hepatic carcinoma (Hildreth et al., 2000; Webster and Cameron, 1967). This may be particularly true in Arctic Canada, where there is little index of sus-picion on the part of medical practitioners, hydatid disease is not notifiable at the national level, and many records do not differentiate between alveolar (E. multilocularis) and cystic (E. granulosus) hydatid disease (Gilbert et al., 2010).

North American strains may have lower zoonotic potential than the European or Asian strains of E. multilocularis. If so, the majority of human cases reported in western Alaska might have been infections with Asian hap-lotypes (Nakao et al., 2009). While it is possible that the low prevalence of human infection in the rest of North America is due to a decreased oppor-tunity for human exposure, this seems unlikely given that many residents of the North (especially Indigenous peoples) hunt, trap, consume untreated surface water, and harvest wild foods. The transmission of cystic hydatid disease continues to occur in northern and Indigenous communities within the range of E. multilocularis in North America (Gilbert et al., 2010; Hil-dreth et al., 2000; Himsworth et al., 2010a). This reinforces the idea that parasite genetic differences might account for the lack of human cases of E. multilocularis observed in North America outside of western Alaska, despite relatively high prevalence in wild canids in the NCR.

11.5. Future Impact of Climate and Landscape ChangeClimate alterations, including global warming, will affect the structure and functioning of parasitic ecosystems (Hoberg, 2010; Hoberg et al., 2008a, 2008b; Parmesan and Yohe, 2003; Polley and Thompson, 2009). These effects will be especially felt in the Arctic where average temperatures have increased at double the rate of the global average in the last 100 years (Kutz et al., 2009a). One consequence of climate change in the north is the altera-tion of restrictive temperatures that limit survival and development times of parasites (Kutz et al., 2009a). The current distribution of E. multilocularis is restricted to the northern hemisphere where the impacts of climate change are already being felt. The distributional restriction may therefore make E. multilocularis highly susceptible to the effects of climate change (Jenkins et al., 2011; Mas-Coma et al., 2008). Already, this parasite is emerging (increasing in distribution and prevalence) in wildlife and human hosts elsewhere in the circumpolar North and is colonising new regions through anthropogenic and natural movements of wild and domestic hosts (Davidson et al., 2012; Eckert et al., 2000; Jenkins et al., 2005, 2012; Schweiger et al., 2007).

The survival of infective eggs of E. multilocularis in the environment is affected by both temperature and moisture. The eggs of E. multilocularis are


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susceptible to desiccation and warmer temperatures, which are currently thought to limit the parasite to the northern hemisphere (Mas-Coma et al., 2008). In a future of climate change, increased precipitation and enhanced snow melting in the north may facilitate survival of the eggs of E. multilocu-laris in the summer, while warmer temperatures may decrease overwinter survival (Mas-Coma et al., 2008). In a warmer North America, the Arctic-adapted strain(s) may see decreases at their southern limit, while the strain(s) present in the NCR may expand northward into the Arctic along with temperate-adapted wildlife hosts colonising northern habitats.

Alterations to the distribution of E. multilocularis may largely be medi-ated through changes in rodent IH distribution and abundance. Climate change may open up previously unsuitable areas (such as the boreal forest) by clearing the way for early successional plant species, supporting higher densities of rodent IHs. Climate change is also predicted to increase an overall precipitation in northwestern North America, which will lead to higher primary productivity and in turn, increased stability and density of rodent populations, facilitating amplified transmission of E. multilocularis on the Arctic mainland. Climate change is also predicted to increase extreme weather events, which may in turn increase the frequency and amplitude of fluctuations in arctic rodent populations. Fluctuating rodent numbers may decrease overall transmission of E. multilocularis, or prevalence may be den-sity-dependent (Rausch and Schiller, 1951). In North America, the preva-lence of E. multilocularis is higher where deer mice were more abundant (Holmes et al., 1971). Anthropogenic landscape changes such as deforesta-tion may also lead to an IH-range expansion in North America. In Europe, rodent and fox distributions are enhanced by deforestation and agricultural practices that create a favourable habitat for rodent species, to which foxes are attracted (Giraudoux et al., 2004; Romig et al., 2006; Viet et al., 1999).

In North America, warming temperatures may also increase interna-tional shipping through the Northwest Passage, enabling further opportuni-ties for translocation of infected rodents and dogs. This is supported by the recent establishment of E. multilocularis on Svalbard in the Norwegian Arctic and in Sweden, most likely by the introduction of suitable rodent hosts from shipping, and infected domestic dogs, respectively (Henttonen et al., 2001; Osterman Lind et al., 2011). The recent identification of a European strain of E. multilocularis in central British Columbia, Canada (a previously non-endemic region) may have occurred as a result of importation of infected red foxes from Europe in the last century or the more recent translocation of an infected dog (Jenkins et al., 2012). In Greenland, where Arctic fox




are already present, increased shipping coupled with warming temperatures may provide an opportunity for more suitable rodent IHs to establish, com-pleting the life cycle requirements of E. multilocularis.

In addition to altering the ecology of IHs, climate change may also affect the distribution and abundance of sylvatic definitive hosts in Alaska, Canada,

Table 2.20 Prevalence [% (n)] of Alveolar Hydatid Disease in People in AlaskaLocation Prevalence [% (n)] Method References

St. Lawrence 33 (233) Casoni skin test* Rausch and Schiller (1956)

Island (SLI) 16 (233) Casoni skin test† Rausch and Schiller (1956)

15 (233) CF Rausch and Schiller (1956)

8 (153) CF Rausch and Schiller (1956)

24 (232) SE Rausch and Schiller (1956)

Gambell, SLI 20 (126) Skin test Rausch and Schiller (1951)

2 (372) SE, X-ray, biopsy Wilson and Rausch (1980)

Savoonga, SLI 28 (106) Skin test Rausch and Schiller (1951)

2 (364) SE, X-ray, biopsy Wilson and Rausch (1980)

Little Diomede 1 (84) SE, X-ray, biopsy Wilson and Rausch (1980)

Wales 2 (131) SE, X-ray, biopsy Wilson and Rausch (1980)

Point Hope 2 (386) SE, X-ray, biopsy Wilson and Rausch (1980)

Noatak <1 (293) SE, X-ray, biopsy Wilson and Rausch (1980)

Kotzebue <1 (1696) SE, X-ray, biopsy Wilson and Rausch (1980)

Kiana <1 (278) SE, X-ray, biopsy Wilson and Rausch (1980)

NR 42 cases SE, X-ray Wilson et al. (1995)

From west to east, then chronologically within a location.CF – complement fixation, SE – serology, NR – not recorded.*Alveolar hydatid antigen.†Cystic hydatid antigen.


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and Greenland. In the early part of the twentieth century in North America and Greenland, red foxes moved north by successfully outcompeting the Arctic fox for food and den sites, possibly as a result of climate alterations (Hersteinsson and Macdonald, 1992; Post et al., 2009). With the encroach-ment of the red fox into Arctic fox territory, there may be an opportu-nity for mixing of the Arctic and southern strains of E. multilocularis, which may differ in pathogenicity, zoonotic potential, and host specificity. Further understanding of the genetic variability, distribution, and zoonotic potential of strains of E. multilocularis is needed in the North and elsewhere in the circumpolar North to assess risks posed by a future of climate and other anthropogenic changes.

12. CONCLUSIONS

12.1. Zoonotic Parasites in the Traditional NorthThe transmission of zoonotic parasites among animals and people in northern North America in the past has reflected close linkages between northern residents and their environment, as well as relatively intact tro-phic relationships among wildlife. For millennia, the harvesting of fish and wildlife for food, together with traditional methods of food prepa-ration, has carried with it risks of food-borne pathogens: for example, Trichinella, Toxoplasma, diphyllobothriid cestodes, and anisakid nematodes. Prior to European colonisation, Indigenous peoples of the Arctic demon-strated traditional knowledge protective against food-borne transmission of parasites, even though historically the specific threat was not identi-fied. For example, bear meat was eaten thoroughly cooked, and wildlife with visible lesions were avoided for human consumption (Rausch, 1968). Interestingly, the last practice might have perpetuated the transmission of E. canadensis in the North if viscera deemed unfit for human consumption were deliberately fed to dogs, the definitive hosts and sources of human infection. In general, close association between people and dogs in the North (sled dogs and free-ranging populations) facilitated human infec-tions with Echinococcus spp. and T. canis (the latter in sub-Arctic regions). Other risk factors for environmentally transmitted parasites in the North included consumption of surface water, harvesting of wild berries, and trapping. Underdeveloped water treatment and sewage infrastructure in the North have likely increased transmission of enteric parasites such as Cryptosporidium and Giardia. Many of these risk factors remain under cur-rent conditions in the North today, and there is evidence that northern




residents remain at higher risk of infection with some parasites than the general North American population (Gilbert et al., 2010).

12.2. Risk Assessment for Zoonotic Parasites in the NorthAs predicted by Rausch (1968), the prevalence of zoonotic helminths, such as Trichinella spp. and anisakid nematodes, as well as Echinococcus spp. and diphyllobothriid cestodes, in Indigenous peoples of the North has declined, likely as a result of improving socioeconomic status, increasing reliance on store-bought foods, and changing dietary preferences (Rausch, 1968, 1972, 1974). However, some zoonotic parasites in the North can have important consequences for the individuals affected due to severity of the disease (e.g. Trichinella, Echinococcus spp.) or health status of the individual (e.g. Toxo-plasma in pregnant women). In addition, surveillance for enteric protozoan parasites (Giardia and Cryptosporidium) in people has only recently been implemented in the USA and Canada, and therefore the public health sig-nificance of these protozoan parasites in the North is largely unknown.

The comprehensive nature of this review provides an unprecedented opportunity for an evidence-based, qualitative risk assessment for the cur-rent public health significance of zoonotic parasites in the North. We have assigned priorities to the nine parasites reviewed (Table 2.21), ranking each parasite from 1 to 4 using the following categories:

barrier. Groups with high host specificity rated lower.-

responds to prevalence in animals and in people, as well as demographic and behavioural risk factors). For example, those parasites that only have opportunities to infect a portion of northern residents, either due to focal geographic distribution or local dietary preferences, rated lower.

-petent people. Parasites that are commonly asymptomatic, or have self-resolving gastrointestinal signs or mild flu-like illness rated lower. Parasites associated with anaphylaxis, abortion, and mortality rated higher.

which treatments are effective and available in the North rated lower, as are those that could be readily diagnosed in the North or by sending samples to southern laboratories. Diseases that require diagnostic equip-ment (such as ultrasound, endoscopy) or procedures (surgery) not read-ily available in the North, sometimes requiring evacuation of the patient, rated higher.


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in a changing North: parasites that are likely to remain restricted geo-graphically and those with life cycles disrupted by environmental change rated lower. Parasites with environmentally susceptible life stages that are likely to benefit in a warmer, wetter North rated higher, as are those that currently show evidence of emergence.

Based on this subjective review process, the zoonotic parasites of most importance in the North from a public health perspective are E. multilocularis, T. gondii, Trichinella spp., and Giardia spp. Alveolar hydatid disease caused by E. multilocularis was prioritised primarily because of severity of disease and difficulty of diagnosis and treatment, especially in remote regions. This parasite is rare outside of western Alaska; however, in a future of climate change, strains of this parasite currently present in western Alaska or in Eurasia might expand their range, or endemic strains might undergo ampli-fication as a result of increased stability and abundance of rodent popula-tions. Elsewhere in the circumpolar North, this parasite is emerging as a result of climate and landscape changes, globalisation, and altered wildlife-pet-people interfaces (Davidson et al., 2012; Eckert et al., 2000; Jenkins et al., 2011; Schweiger et al., 2007).

Based on a low-IH specificity and current evidence of high levels of human exposure in some regions of the North, T. gondii may well be ‘the most important parasitic infection in the North American Arctic’ (Hotez, 2010). However, the prevalence of toxoplasmosis is not uniform across the North; indeed, in most regions other than Nunavik, Canada, prevalence in people is on par or lower than the North American average (Table 2.5). Despite its potential public health importance, transmission of T. gondii remains enigmatic at high latitudes. The role of oocyst transmission of Toxo-plasma (relative to food-borne routes) is not clear in tundra regions where wild and domestic felids are uncommon; however, residents of coastal communities could become infected with oocysts contaminating marine environments. There is some evidence in the Norwegian Arctic that cli-mate change may be enhancing the transmission of toxoplasmosis in Arctic marine systems due to enhanced survival of oocysts transported from sub-Arctic regions and amplification of filter-feeding invertebrate populations, which serve as transport hosts for oocysts ( Jensen et al., 2010).

Giardia and Trichinella together ranked third in terms of public health priority. Giardia was prioritised due to the disproportionately high number of cases reported in people in the North, and the high probability of under-diagnosis due to the mild or asymptomatic nature of infection (Scallan et al.,




2011). It is not known how many outbreaks and cases of giardiasis are of animal versus human origin; however, pets and ‘urban’ wildlife may play a role in maintaining and transmitting zoonotic genotypes of Giardia within human communities. Trichinella remains an important public health consid-eration due to the possibility of large outbreaks resulting from food-sharing, severe and even fatal consequences of disease, and evidence of ongoing exposure across the North. Likewise, cystic hydatid disease (E. canadensis) was ranked moderately high because of the potential severity of the disease, difficulty in diagnosis and treatment in remote areas, and evidence of ongo-ing exposure across the North.

For two environmentally transmitted parasites, Toxocara and Cryptospo-ridium, both human and animal cases currently appear to be rare in the Arctic. For Toxocara, development and survival of environmental stages has likely been limited historically by abiotic conditions in the North. For Cryptosporidium, there may be also be environmental tolerance limitations; alternatively, there may not have been sufficient densities of human and livestock populations to support high levels of amplification of this pro-tozoan in the North. Both these parasites are flagged to emerge in a more permissive and populated northern environment. Anisakidosis and diphyl-lobothriosis ranked the lowest for concern due to evidence of low levels of human transmission, mild disease, and the possibility that climate change may disrupt marine cycles of transmission. It is important to note that this risk assessment was primarily based on public health significance versus animal health or trade criteria. Both of these fish-borne parasites may be of increasing concern as fish are marketed for export from the North, and visi-tors come into the North and sample local foods without local knowledge of food safety considerations.

12.3. Risk MitigationRisk mitigation for some of these diseases in northern communities is already in place and showing evidence of success. For endemic helminth zoono-ses, exposure in people in the North appears to be declining. In Alaska, this holds true for diseases for which there are physician-reporting systems and laboratory-based surveillance (trichinellosis, alveolar and cystic hydatid disease – Figs. 2.13, 2.23, and 2.26). In Canada, recent serosurveys over the last decade in Nunavik and the James Bay Cree regions of QC, Nunatsiavut in NL, and the Inuvialuit settlement region in the NT, collectively suggest that exposure to Trichinella and Echinococcus is low and/or declining in northeastern Canada (Tables 2.9, 2.11, and 2.18) (Campagna et al., 2011; Egeland et al., 2010a,


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2010b; Lévesque et al., 2007; Messier et al., 2012; Sampasa-Kanyinga et al., 2012). Other than reported cases of cystic hydatid disease in the 1950s, little surveillance has occurred in people in sub-Arctic regions in western Canada, including the northern half of the Prairie Provinces. A recent serosurvey for zoonotic parasites in one Dene community in northern SK suggests that these diseases may persist in these communities at levels higher than those currently reported in Inuit and Cree in northeastern Canada (Schurer et al., 2013).

Declines in these endemic helminth zoonoses are in part a consequence of changes in dietary preference and availability of processed foods, and the passing of sled dogs as a primary method of transportation in the North. However, some of these declines may be a result of public health messaging and programming, such as the NTPP (Nunavik Trichinellosis Prevention Programme), which screens harvested walrus for trichinellosis prior to con-sumption, and screening of pregnant Nunavik women for toxoplasmosis (Lavoie et al., 2008; Proulx et al., 2002). Another success story is the impact of regular anthelminthic treatment of dogs on St Lawrence Island, Alaska, which led to significant reductions in prevalence of alveolar hydatid cysts in rodents as an indicator of environmental egg contamination (Rausch et al., 1990b). In many northern and Indigenous communities, however, access to veterinary medical and veterinary public health services remains a chal-lenge (Brook et al., 2010; Jenkins et al., 2011). In addition, evaluation of the success of these interventions is seldom performed and critically needed to motivate funding for and focus on such programmes.

Public education and targeted interventions are key to mitigating risks of zoonotic parasites (Schwabe, 1986). The most successful approaches have taken into account the undeniable benefits of wildlife as high-quality main-stays of northern diets, and the ongoing challenges of maintaining security and safety of food and water in a remote and harsh environment. Public health interventions for the control of environmentally transmitted parasites include drinking water and sewage treatment, as well as environmental hygiene and dog population control. As true of today as it was 4 decades ago, ‘control of zoonotic diseases in arctic regions can best be achieved through education and improvement of the standard of living, but because some customs change only with difficulty, rapid progress is not to be expected’ (Rausch, 1968).

12.4. Zoonotic Parasites in a North in TransitionRapid and accelerating environmental change may already be altering the distribution and transmission of zoonotic diseases currently present in the North. For example, T. canis has now been reported at latitudes greater than




60°N in areas of western Canada where it was not detected in studies 35 years previously ( Jenkins et al., 2011; Salb et al., 2008; Unruh et al., 1973). While there are uncertainties about the magnitude and variability of climate changes in northern Canada, the overall direction of change in the terrestrial Arctic appears to be warmer, wetter, with an increased severity and frequency of extreme climatic events, especially for the western Arctic. Changes in marine systems appear to be greater than those in terrestrial sys-tems, with enhanced velocity of change as well as shifts in phenology (Bur-rows et al., 2011). When considering the effects of climate and landscape changes, as well as other drivers of emerging diseases, on the ecology of zoonotic diseases in the North, some common themes are apparent among the mechanisms of disease emergence.

For parasites with largely food-borne transmission routes in the North (such as Trichinella, Toxoplasma, anisakid nematodes, and diphyllobothriid cestodes), effects of climate change will be largely linked to changes in the distribution and abundance of wildlife reservoirs and altered interfaces between wildlife and people. These changes are happening against a com-plex backdrop of social and cultural change that may decrease zoonotic risks due to these parasites, independently of the effects of environmental change on transmission in sylvatic cycles. In contrast, environmentally transmitted

Table 2.21 Qualitative Risk Assessment From a Public Health Perspective for the Nine Parasitic Zoonoses in the North Considered in this Review

Zoonotic potential

Human exposure

Disease severity

Di"culty of dx/tx Emergence Total

Alveolar hydatid*

2 1 4 4 3 14

Anisakidosis 2 1 1 3 2 9Cryptospo-

ridiosis3 2 1 2 3 11

Cystic hydatid†

2 2 3 3 1 11

Diphylloboth-riosis

2 2 1 1 2 8

Giardiasis 3 4 1 1 3 12Toxocariasis 2 1 2 2 3 10Toxoplasmosis 4 3 2 2 2 13Trichinellosis 3 2 3 3 1 12

For each criterion, diseases were ranked from 1 (lowest) to 4 (highest).dx – diagnosis, tx – treatment.*Echinococcus multilocularis.†E. canadensis (cervid strain of E. granulosus).


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parasites (such as Giardia, Cryptosporidium, Toxocara, and oocysts of Toxo-plasma) may now be coming into their own in an increasingly connected and hospitable North. Parasites that undergo water-borne transmission (Giardia, Cryptosporidium, and possibly Toxoplasma) will be influenced greatly by changes in regional hydrology and frequency of extreme rainfall events; human exposure to water-borne diseases will largely rely on the resilience of water treatment infrastructure and availability of treated water. Pathogens with life stages that undergo mandatory and often temperature-dependent development in the environment (such as Toxoplasma, Toxocara, anisakid nematodes, and diphyllobothriid cestodes) will likely undergo accelerated development in endemic areas, although this may trade off against decreased survival at warmer temperatures in summer.

This review process has enabled more accurate determination of north-ern distributions of parasites and their distributional limits based on the best available knowledge in the published literature, and allows us to describe current and future vulnerabilities for northern North America. For example, parasites with environmental life stages that are currently excluded from Arctic regions of mainland North America (D. latum, T. canis, and possibly Cryptosporidium) might well move north, along with domestic livestock, pets, and wildlife that are currently better established in sub-Arc-tic and temperate regions. In addition, Greenland appears to be currently free of several zoonotic parasites (including E. granulosus, E. multilocularis, and T. canis). Echinococcus multilocularis has recently been identified in newly endemic regions in the circumpolar North, likely as a result of importation of domestic dogs (Davidson et al., 2012). Given the connectivity of once remote northern locations and an increasingly permissive climate, main-tenance of country freedom status might well rely on import regulations mandating prophylactic treatment and screening of imported animals.

12.5. Future Needs for Research and Surveillance of Zoonotic Parasites in the NorthPerhaps the most important outcome of this review process is identification of knowledge gaps regarding the diversity and health significance of zoo-notic parasites in the North. Until recently, many were thought to be the same parasite species as those in animals and people at temperate latitudes (i.e. freeze-susceptible T. spiralis versus freeze-tolerant northern Trichinella species). Until 1960, E. multilocularis and E. granulosus, which we now know to have very different clinical syndromes and prognoses, were thought to be the same species, and genetic diversity across the circumpolar distribution




of E. multilocularis has only recently been recognised. Protozoans, especially Giardia spp., may be one of the most important causes of enteric disease in northern human populations; however, molecular and epidemiologi-cal characterisation to determine source of infection is seldom performed. Such investigations are necessary to determine zoonotic potential and to aid in source attribution in human clinical cases and outbreaks. In addition, molecular databases and ‘fingerprints’ are needed to detect the emergence of new zoonoses and to track movements of strains and species of parasite zoonoses around the globe (Davidson et al., 2012; Jenkins et al., 2012). This in turn provides compelling evidence to motivate and prioritise risk mitiga-tion measures, such as targeted food safety recommendations, or regulations for import and export of animals and animal products. Basic survey and inventory of parasites present in the North, and those poised on its doorstep, are critically needed in order to detect and predict changes in patterns of distribution and transmission of zoonotic parasites (Hoberg, 2010; Hoberg et al., 2008a, 2008b, 2012, in press).

While this review has focused on the public health significance of zoo-notic parasites, the impact of endemic and potentially introduced parasites on the health of northern wildlife populations important for ecological, cultural, and socioeconomic reasons is almost completely unknown. We have also identified gaps in surveillance for zoonotic parasites in different human populations in the North. For example, most surveillance efforts have focused on Indigenous groups; non-indigenous northern residents might experience different risk factors and would be a useful out-group for comparison. In addition, non-Indigenous residents may be at increased risk of exposure due to lack of protective traditional knowledge, and may experience more severe outcomes of infection with northern parasites for which they have had little historical exposure, such as E. canadensis (McMa-nus et al., 2002; Rausch, 2003).

Compelling evidence (such as cost-benefit analyses) is needed to moti-vate public health policy makers to prioritise parasites in the light of other infectious and chronic diseases facing the North. In many ways, the obser-vations of Robert Rausch, to whom this review is dedicated, are as relevant today as they were 60 years ago, when his early publications led to the first recognition of the importance of Arctic zoonoses. Prior to this, the focus in the medical literature on infectious diseases in the North was almost entirely on diseases directly transmissible from person to person (Rausch, 1968). This trend is still observable today; for example, at the 14th International Congress on Circumpolar Health in 2009, infectious diseases of northern


Arctic Zoonoses 177


importance on the agenda were tuberculosis, respiratory and reproductive diseases, hepatitis, Helicobacter pylori, and antibiotic resistant bacteria (http://icch2009.circumpolarhealth.org/schedule/programme/). The importance of these infectious diseases, along with chronic diseases such as diabetes, cancer, and cardiovascular dysfunction, is undeniable. We forget parasitic zoonoses at our peril, however, as they are more likely to emerge, or re-emerge, in northern populations challenged by other infectious and chronic diseases. In addition, the perceived threat of parasitic zoonoses cannot be allowed to drive Indigenous and northern residents away from their ties to the land. Maintaining this relationship requires an increased focus on the preventable nature of zoonotic transmission of parasites through public education, and interventions that address critical determinants of health in northern peoples. Finally, there is a need to explore the potential for emer-gence of zoonotic parasites in tandem with the potential for adaptation on the part of northern residents and wildlife in a North at the interface between tradition and transition.

ACKNOWLEDGEMENTSWe acknowledge the contributions of Brent Wagner, Juliane Deubner, Aaron Genest, Lena Measures, Kimberlee Beckmen, Kelly Konecsni (curator of the Canada Database of Animal Parasites maintained at the Canadian Food Inspection Agency Centre for Food-borne and Animal Parasites), and the Notifiable Diseases and Field Surveillance Section, Surveillance and Epidemiology Division, Centre for Communicable Diseases and Infection Control, Public Health Agency of Canada. Funding for this project was provided by: Canadian Foundation for Innovation Leaders Opportunity Fund, Natural Sciences and Engineering Research Council, Public Health and the Agricultural Rural Ecosystem Training Program (Canadian Institutes of Health Research Strategic Training Initiative in Health Research), Public Health Agency of Canada, Saskatchewan Health Research Foundation, University of Saskatchewan, and the Western College of Veterinary Medicine, Saskatoon, SK, Canada.

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