Hostname: page-component-586b7cd67f-vdxz6 Total loading time: 0 Render date: 2024-11-28T00:02:27.310Z Has data issue: false hasContentIssue false
  • English
  • Français

Spatio-temporal variations and age effect on Toxoplasma gondii seroprevalence in seals from the Canadian Arctic

Published online by Cambridge University Press:  04 August 2011

A. SIMON ,
M. CHAMBELLANT ,
B. J. WARD ,
M. SIMARD ,
J. F. PROULX ,
B. LEVESQUE ,
M. BIGRAS-POULIN ,
A. N. ROUSSEAU  and
N. H. OGDEN
A. SIMON*
Affiliation:
Faculté de médecine vétérinaire, Université de Montréal, Pathologie et microbiologie Saint-Hyacinthe, Québec, Canada
M. CHAMBELLANT
Affiliation:
Fisheries and Oceans Canada, Fisheries and Oceans, Winnipeg, Manitoba, Canada University of Manitoba, Department of Biological Sciences, Winnipeg, Manitoba, Canada
B. J. WARD
Affiliation:
Research Institute of the McGill University Health Centre, Montreal General Hospital, Montreal, Quebec, Canada
M. SIMARD
Affiliation:
Makivik Corporation, Nunavik Research Center, Kuujjuaq, Quebec, Canada
J. F. PROULX
Affiliation:
Nunavik Regional Board of Health and Social Services, Direction de la Santé Publique, Kuujjuaq, Quebec, Canada
B. LEVESQUE
Affiliation:
Centre de Recherche du Centre Hospitalier Universitaire de Québec, Axe Santé des Populations et Environnement, Québec, Québec, Canada Institut National de Santé Publique du Québec, Direction de la Santé Environnementale et de la Toxicologie, Québec, Québec, Canada
M. BIGRAS-POULIN
Affiliation:
Faculté de médecine vétérinaire, Université de Montréal, Pathologie et microbiologie Saint-Hyacinthe, Québec, Canada
A. N. ROUSSEAU
Affiliation:
Institut National de Recherche Scientifique, Centre Eau Terre Environnement, Québec, Québec, Canada
N. H. OGDEN
Affiliation:
Zoonoses Division, Centre for Food-borne, Environmental and Zoonotic Infectious Diseases, Public Health Agency of Canada, Saint-Hyacinthe, Quebec, Canada
*
*Corresponding author: Groupe de recherche en épidémiologie des zoonoses et santé publique, Faculté de médecine vétérinaire, Université de Montréal, 3200 Sicotte, C.P. 5000, Saint-Hyacinthe, J2S 7C6, Québec, Canada. Tel: +1(450) 773 8521 ext. 0082. Fax: +1(450) 778 8129. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Toxoplasmosis is a significant public health threat for Inuit in the Canadian Arctic. This study aimed to investigate arctic seals as a possible food-borne source of infection. Blood samples collected from 828 seals in 7 Canadian Arctic communities from 1999 to 2006 were tested for Toxoplasma gondii antibodies using a direct agglutination test. Polymerase chain reaction (PCR) was used to detect T. gondii DNA in tissues of a subsample of seals. Associations between seal age, sex, species, diet, community and year of capture, and serological test results were investigated by logistic regression. Overall seroprevalence was 10·4% (86/828). All tissues tested were negative by PCR. In ringed seals, seroprevalence was significantly higher in juveniles than in adults (odds ratio=2·44). Overall, seroprevalence varied amongst communities (P=0·0119) and by capture year (P=0·0001). Our study supports the hypothesis that consumption of raw seal meat is a significant source of infection for Inuit. This work raises many questions about the mechanism of transfer of this terrestrial parasite to the marine environment, the preponderance of infection in younger animals and the natural course of infection in seals. Further studies to address these questions are essential to fully understand the health risks for Inuit communities.

Keywords

Toxoplasma gondiisealsCanadian Arcticwild felidswaterborne transmission
Type
Research Article
Information
Parasitology , Volume 138 , Issue 11 , September 2011 , pp. 1362 - 1368
Copyright
Copyright © Cambridge University Press 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Appelbee, A. J., Thompson, R. C. and Olson, M. E. (2005). Giardia and Cryptosporidium in mammalian wildlife–current status and future needs. Trends in Parasitology 21, 370–376.CrossRefGoogle ScholarPubMed
Arkush, K. D., Miller, M. A., Leutenegger, C. M., Gardner, I. A., Packham, A. E., Heckeroth, A. R., Tenter, A. M., Barr, B. C. and Conrad, P. A. (2003). Molecular and bioassay-based detection of Toxoplasma gondii oocyst uptake by mussels (Mytilus galloprovincialis). International Journal for Parasitology 33, 1087–1097.CrossRefGoogle ScholarPubMed
Banfield, A. W. F. (1974). The Mammals of Canada, University of Toronto Press Toronto, Canada.Google Scholar
Born, E. W., Teilmann, J., Acquarone, M. and Riget, F. F. (2004). Habitat use of ringed seals (Phoca hispida) in the North Water Area (North Baffin Bay). Arctic 57, 129–142.CrossRefGoogle Scholar
Cabezon, O., Hall, A. J., Vincent, C., Pabon, M., Garcia-Bocanegra, I., Dubey, J. P. and Almeria, S. (2011). Seroprevalence of Toxoplasma gondii in North-eastern Atlantic harbor seal (Phoca vitulina vitulina) and grey seal (Halichoerus grypus). Veterinary Parasitology 90, 225–260.Google Scholar
Cabezon, O., Resendes, A. R., Domingo, M., Raga, J. A., Agusti, C., Alegre, F., Mons, J. L., Dubey, J. P. and Almeria, S. (2004). Seroprevalence of Toxoplasma gondii antibodies in wild dolphins from the Spanish Mediterranean coast. Journal of Parasitology 90, 643–644.CrossRefGoogle ScholarPubMed
Campagna, S., Levesque, B., Anassour-Laouan-Sidi, E., Cote, S., Serhir, B., Ward, B. J., Libman, M. D., Drebot, M. A., Makowski, K., Andonova, M., Ndao, M. and Dewailly, E. (2011). Seroprevalence of 10 zoonotic infections in 2 Canadian Cree communities. Diagnostic Microbiology and Infectious Disease 70, 191–199.CrossRefGoogle ScholarPubMed
Conrad, P. A., Miller, M. A., Kreuder, C., James, E. R., Mazet, J., Dabritz, H., Jessup, D. A., Gulland, F. and Grigg, M. E. (2005). Transmission of Toxoplasma: clues from the study of sea otters as sentinels of Toxoplasma gondii flow into the marine environment. International Journal of Parasitology 35, 1155–1168.Google Scholar
Dubey, J. P. (2010). Toxoplasmosis of Animals and Humans, 2nd Edn. CRC Press, Inc., Boca Raton, Fl, USA.Google Scholar
Dubey, J. P., Fair, P. A., Bossartt, G. D., Hill, D., Fayer, R., Sreekumar, C., Kwok, O. C. and Thulliez, P. (2005). A comparison of several serologic tests to detect antibodies to Toxoplasma gondii in naturally exposed bottlenose dolphins (Tursiops truncatus). Journal of Parasitology 91, 1074–1081.CrossRefGoogle ScholarPubMed
Dubey, J. P., Zarnke, R., Thomas, N. J., Wong, S. K., Van Bonn, W., Briggs, M., Davis, J. W., Ewing, R., Mense, M., Kwok, O. C., Romand, S. and Thulliez, P. (2003). Toxoplasma gondii, Neospora caninum, Sarcocystis neurona, and Sarcocystis canis-like infections in marine mammals. Veterinary Parasitology 116, 275–296.CrossRefGoogle ScholarPubMed
Forbes, L. B., Measures, L. and Gajadhar, A. (2009). Infectivity of Toxoplasma gondii in northern traditional (country) foods prepared with meat from experimentally infected seals. Journal of Food Protection 72, 1756–1760.CrossRefGoogle ScholarPubMed
Gajadhar, A. A., Measures, L., Forbes, L. B., Kapel, C. and Dubey, J. P. (2004). Experimental Toxoplasma gondii infection in grey seals (Halichoerus grypus). Journal of Parasitology 90, 255–259.CrossRefGoogle ScholarPubMed
Gyorkos, T. W. (1980). Serological investigation for five selected parasitic infections in Inuvik and Arctic Bay/Strathcona Sound, Nothwest Territories. Canada Diseases Weekly Report 6, 134–136.Google Scholar
Hill, D. E., Chirukandoth, S., Dubey, J. P., Lunney, J. K. and Gamble, H. R. (2006). Comparison of detection methods for Toxoplasma gondii in naturally and experimentally infected swine. Veterinary Parasitology 141, 9–17.CrossRefGoogle ScholarPubMed
Holst, M., Stirling, I. and Calvert, W. (1999). Age structure and reproductive rates of ringed seals (Phoca hispida) on the northwestern coast of Hudson Bay in 1991 and 1992. Marine Mammal Science 15, 1357–1364.Google Scholar
Jardine, J. E. and Dubey, J. P. (2002). Congenital toxoplasmosis in a Indo-Pacific bottlenose dolphin (Tursiops aduncus). Journal of Parasitology 88, 197–199.Google Scholar
Jensen, S. K., Aars, J., Lydersen, C., Kovacs, K. M. and Asbakk, K. (2010). The prevalence of Toxoplasma gondii in polar bears and their marine mammal prey: evidence for a marine transmission pathway? Polar Biology 33, 599–606.CrossRefGoogle Scholar
Jones, J. L. and Dubey, J. P. (2010). Waterborne toxoplasmosis–recent developments. Experimental Parasitology 124, 10–25.CrossRefGoogle ScholarPubMed
Kasper, D. C., Sadeghi, K., Prusa, A. R., Reischer, G. H., Kratochwill, K., Forster-Waldl, E., Gerstl, N., Hayde, M., Pollak, A. and Herkner, K. R. (2009). Quantitative real-time polymerase chain reaction for the accurate detection of Toxoplasma gondii in amniotic fluid. Diagnostic Microbiology and Infectious Disease 63, 10–15.CrossRefGoogle ScholarPubMed
Labelle, P., Dubey, J. P., Mikaelian, I., Blanchette, N., Lafond, R., St-Onge, S. and Martineau, D. (2001). Seroprevalence of antibodies to Toxoplasma gondii in lynx (Lynx canadensis) and bobcats (Lynx rufus) from Quebec, Canada. Journal of Parasitology 87, 1194–1196.CrossRefGoogle ScholarPubMed
Lambourn, D. M., Jeffries, S. J. and Dubey, J. P. (2001). Seroprevalence of Toxoplasma gondii in harbor seals (Phoca vitulina) in southern Puget Sound, Washington. Journal of Parasitology 87, 1196–1197.CrossRefGoogle Scholar
Leclair, D. and Doidge, W. (1998). Seropositive Cases of Toxoplasmosis in Nunavik wildlife. Nunavik Research Centre, Makivik Corporation, Kuujjuaq, Canada.Google Scholar
Levesque, B., Messier, V., Bonnier-Viger, Y., Couillard, M., Cote, S., Ward, B. J., Libman, M. D., Gingras, S., Dick, D. and Dewailly, E. (2007). Seroprevalence of zoonoses in a Cree community (Canada). Diagnostic Microbiology and Infectious Disease 59, 283–286.CrossRefGoogle Scholar
Lindsay, D. S., Collins, M. V., Mitchell, S. M., Wetch, C. N., Rosypal, A. C., Flick, G. J., Zajac, A. M., Lindquist, A. and Dubey, J. P. (2004). Survival of Toxoplasma gondii oocysts in Eastern oysters (Crassostrea virginica). Journal of Parasitology 90, 1054–1057.Google Scholar
Lindsay, D. S. and Dubey, J. P. (2009). Long-term survival of Toxoplasma gondii sporulated oocysts in seawater. Journal of Parasitology 95, 1019–1020.CrossRefGoogle ScholarPubMed
Massie, G. N., Ware, M. W., Villegas, E. N. and Black, M. W. (2010). Uptake and transmission of Toxoplasma gondii oocysts by migratory, filter-feeding fish. Veterinary Parasitology 169, 296–303.CrossRefGoogle ScholarPubMed
Measures, L. N., Dubey, J. P., Labelle, P. and Martineau, D. (2004). Seroprevalence of Toxoplasma gondii in Canadian pinnipeds. Journal of Wildlife Diseases 40, 294–300.Google Scholar
Messier, V., Levesque, B., Proulx, J. F., Rochette, L., Libman, M. D., Ward, B. J., Serhir, B., Couillard, M., Ogden, N. H., Dewailly, E., Hubert, B., Dery, S., Barthe, C., Murphy, D. and Dixon, B. (2009). Seroprevalence of Toxoplasma gondii among Nunavik Inuit (Canada). Zoonoses and Public Health 56, 188–197.Google Scholar
Mikaelian, I., Boisclair, J., Dubey, J. P., Kennedy, S. and Martineau, D. (2000). Toxoplasmosis in beluga whales (Delphinapterus leucas) from the St Lawrence estuary: two case reports and a serological survey. Journal of Comparative Pathology 122, 73–76.Google Scholar
Miller, M., Conrad, P., James, E. R., Packham, A., Toy-Choutka, S., Murray, M. J., Jessup, D. and Grigg, M. (2008 a). Transplacental toxoplasmosis in a wild southern sea otter (Enhydra lutris nereis). Veterinary Parasitology 153, 12–18.Google Scholar
Miller, M. A., Byrne, B. A., Jang, S. S., Dodd, E. M., Dorfmeier, E., Harris, M. D., Ames, J., Paradies, D., Worcester, K., Jessup, D. A. and Miller, W. A. (2010). Enteric bacterial pathogen detection in southern sea otters (Enhydra lutris nereis) is associated with coastal urbanization and freshwater runoff. Veterinary Research 41, 1–13.CrossRefGoogle ScholarPubMed
Miller, M. A., Miller, W. A., Conrad, P. A., James, E. R., Melli, A. C., Leutenegger, C. M., Dabritz, H. A., Packham, A. E., Paradies, D., Harris, M., Ames, J., Jessup, D. A., Worcester, K. and Grigg, M. E. (2008 b). Type×Toxoplasma gondii in a wild mussel and terrestrial carnivores from coastal California: new linkages between terrestrial mammals, runoff and toxoplasmosis of sea otters. International Journal for Parasitology 38, 1319–1328.CrossRefGoogle Scholar
Oksanen, A., Tryland, M., Johnsen, K. and Dubey, J. P. (1998). Serosurvey of Toxoplasma gondii in North Atlantic marine mammals by the use of agglutination test employing whole tachyzoites and dithiothreitol. Comparative Immunology, Microbiology and Infectious Diseases 21, 107–114.Google Scholar
Opsteegh, M., Swart, A., Fonville, M., Dekkers, L. and van der Giessen, J. (2011). Age-related Toxoplasma gondii seroprevalence in Dutch wild boar inconsistent with lifelong persistence of antibodies. PLoS One 6, e16240. doi: 10.1371/journal.pone.0016240.Google Scholar
Prestrud, K. W., Asbakk, K., Fuglei, E., Mork, T., Stien, A., Ropstad, E., Tryland, M., Gabrielsen, G. W., Lydersen, C., Kovacs, K. M., Loonen, M. J., Sagerup, K. and Oksanen, A. (2007). Serosurvey for Toxoplasma gondii in arctic foxes and possible sources of infection in the high Arctic of Svalbard. Veterinary Parasitology 150, 6–12.CrossRefGoogle ScholarPubMed
Resendes, A. R., Almeria, S., Dubey, J. P., Obon, E., Juan-Salles, C., Degollada, E., Alegre, F., Cabezon, O., Pont, S. and Domingo, M. (2002). Disseminated toxoplasmosis in a Mediterranean pregnant Risso's dolphin (Grampus griseus) with transplacental fetal infection. Journal of Parasitology 88, 1029–1032.CrossRefGoogle Scholar
Robertson, L. J. (2007). The potential for marine bivalve shellfish to act as transmission vehicles for outbreaks of protozoan infections in humans: a review. International Journal of Food Microbiology 120, 201–216.CrossRefGoogle ScholarPubMed
Stewart, R. E. A., Stewart, B. E., Stirling, I. and Street, E. (1996). Counts of growth layer groups in cementum and dentine in ringed seals (Phoca hispida). Marine Mammal Science 12, 383–401.CrossRefGoogle Scholar
Tanner, C. E., Staudt, M., Adamowski, R., Lussier, M., Bertrand, S. and Prichard, R. K. (1987). Seroepidemiological study for five different zoonotic parasites in northern Quebec. Canadian Journal of Public Health 78, 262–266.Google ScholarPubMed
Tenter, A. M., Heckeroth, A. R. and Weiss, L. M. (2000). Toxoplasma gondii: from animals to humans. International Journal for Parasitology 30, 1217–1258.CrossRefGoogle ScholarPubMed
Thomas, N. J., Dubey, J. P., Lindsay, D. S., Cole, R. A. and Meteyer, C. U. (2007). Protozoal meningoencephalitis in sea otters (Enhydra lutris): a histopathological and immunohistochemical study of naturally occurring cases. Journal of Comparative Pathology 137, 102–121. doi: DOI 10.1016/j.jcpa.2007.05.001.CrossRefGoogle ScholarPubMed
Vincent-Chambellant, M. (2010). Ecology of ringed seals (Phoca hispida). Ph. D. thesis, University of Manitoba, Winnipeg, Canada.Google Scholar