Toxoplasma gondii DNA in Tissues of Anadromous Arctic Charr, Salvelinus alpinus, Collected From Nunavik, Québec, Canada.
Toxoplasma gondii
Arctic charr
PCR
fish
foodborne transmission
Journal
Zoonoses and public health
ISSN: 1863-2378
Titre abrégé: Zoonoses Public Health
Pays: Germany
ID NLM: 101300786
Informations de publication
Date de publication:
09 Sep 2024
09 Sep 2024
Historique:
revised:
31
07
2024
received:
29
04
2024
accepted:
01
08
2024
medline:
10
9
2024
pubmed:
10
9
2024
entrez:
10
9
2024
Statut:
aheadofprint
Résumé
Toxoplasma gondii is a very common zoonotic parasite in humans and animals worldwide. Human seroprevalence is high in some regions of Canada's North and is thought to be associated with the consumption of traditionally prepared country foods, such as caribou, walrus, ringed seal and beluga. While numerous studies have reported on the prevalence of T. gondii in these animals, in the general absence of felid definitive hosts in the North there has been considerable debate regarding the source of infection, particularly in marine mammals. It has been proposed that fish could be involved in this transmission. The objectives of the present study were to perform a targeted survey to determine the prevalence of T. gondii DNA in various tissues of anadromous Arctic charr sampled in Nunavik, Québec, and to investigate the possible role of this commonly consumed fish in the transmission of infection to humans and marine mammals in Canada's North. A total of 126 individual Arctic charr were sampled from several sites in Nunavik, and various tissues were tested for the presence of T. gondii DNA using PCR. Overall, 12 out of 126 (9.5%) Arctic charr tested in the present study were PCR-positive, as confirmed by DNA sequencing. Brain tissue was most commonly found to be positive, followed by heart tissue, while none of the dorsal muscle samples tested were positive. Although the presence of T. gondii DNA in brain and heart tissues of Arctic charr is very intriguing, infection in these fish, and their possible role in the transmission of this parasite to humans and marine mammals, will need to be confirmed using mouse bioassays. Arctic charr are likely exposed to T. gondii through the ingestion of oocysts transported by surface water and ocean currents from more southerly regions where the definitive felid hosts are more abundant. If infection in Arctic charr can be confirmed, it is possible that these fish could play an important role in the transmission of toxoplasmosis to Inuit, either directly through the consumption of raw fish or indirectly through the infection of fish-eating marine mammals harvested as country foods.
Sections du résumé
BACKGROUND
BACKGROUND
Toxoplasma gondii is a very common zoonotic parasite in humans and animals worldwide. Human seroprevalence is high in some regions of Canada's North and is thought to be associated with the consumption of traditionally prepared country foods, such as caribou, walrus, ringed seal and beluga. While numerous studies have reported on the prevalence of T. gondii in these animals, in the general absence of felid definitive hosts in the North there has been considerable debate regarding the source of infection, particularly in marine mammals. It has been proposed that fish could be involved in this transmission.
AIMS
OBJECTIVE
The objectives of the present study were to perform a targeted survey to determine the prevalence of T. gondii DNA in various tissues of anadromous Arctic charr sampled in Nunavik, Québec, and to investigate the possible role of this commonly consumed fish in the transmission of infection to humans and marine mammals in Canada's North.
METHODS AND RESULTS
RESULTS
A total of 126 individual Arctic charr were sampled from several sites in Nunavik, and various tissues were tested for the presence of T. gondii DNA using PCR. Overall, 12 out of 126 (9.5%) Arctic charr tested in the present study were PCR-positive, as confirmed by DNA sequencing. Brain tissue was most commonly found to be positive, followed by heart tissue, while none of the dorsal muscle samples tested were positive.
CONCLUSIONS
CONCLUSIONS
Although the presence of T. gondii DNA in brain and heart tissues of Arctic charr is very intriguing, infection in these fish, and their possible role in the transmission of this parasite to humans and marine mammals, will need to be confirmed using mouse bioassays. Arctic charr are likely exposed to T. gondii through the ingestion of oocysts transported by surface water and ocean currents from more southerly regions where the definitive felid hosts are more abundant. If infection in Arctic charr can be confirmed, it is possible that these fish could play an important role in the transmission of toxoplasmosis to Inuit, either directly through the consumption of raw fish or indirectly through the infection of fish-eating marine mammals harvested as country foods.
Banques de données
RefSeq
['PP792698-PP792700', 'PP795922-PP795930']
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024 His Majesty the King in Right of Canada and The Author(s). Zoonoses and Public Health published by Wiley‐VCH GmbH. Reproduced with the permission of the Minister of Health Canada and the Environment and the Fight Against Climate Change.
Références
Aakool, A. A., and S. J. Abidali. 2016. “Molecular Detection of Toxoplasma gondii in Native Freshwater Fish Cyprinuscarpio in Wasit Province Iraq.” International Journal of Scientific and Engineering Research 4: 7–10.
Allaire, J., L. Johnson‐Down, M. Little, P. Ayotte, and M. Lemire. 2021. Country and Market Food Consumption and Nutritional Status. Nunavik Inuit Health Survey 2017 Qanuilirpitaa? How Are We now? Quebec: Nunavik Regional Board of Health and Social Services (NRBHSS) & Institut National de Santé Publique du Québec (INSPQ).
Almeria, S., and J. P. Dubey. 2021. “Foodborne Transmission of Toxoplasma gondii Infection in the Last Decade. An Overview.” Research in Veterinary Science 135: 371–385.
Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. “Basic Local Alignment Search Tool.” Journal of Molecular Biology 215: 403–410.
Bahia‐Oliveira, L., J. Gomez‐Marin, and K. Shapiro. 2017. “Toxoplasma gondii.” In Water and Sanitation for the 21st Century: Health and Microbiological Aspects of Excreta and Wastewater Management (Global Water Pathogen Project) (R. Fayer & W. Jakubowski (eds), Part 3: Specific Excreted Pathogens: Environmental and Epidemiology Aspects—Section 3: Protists), Michigan State University, edited by J. B. Rose and B. Jiménez‐Cisneros. E. Lansing, MI: UNESCO. https://doi.org/10.14321/waterpathogens.37.
Bolduc, S., M. Lemire, J.‐É. Tremblay, et al. 2024. “Assessment of Inter‐Regional Dietary Differences in Anadromous Arctic Char (Salvelinus alpinus) in Nunavik, Canada, and Links With Flesh Quality Indicators.” Arctic Science 10: 372–385. https://doi.org/10.1139/AS‐2023‐0018.
Bouchard, É., R. Sharma, A. Hernández‐Ortiz, et al. 2022. “Are Foxes (Vulpes spp.) Good Sentinel Species for Toxoplasma gondii in Northern Canada?” Parasites & Vectors 15: 115. https://doi.org/10.1186/s13071‐022‐05229‐3.
Burnham, K. P., D. R. Anderson, and K. P. Huyvaert. 2011. “AIC Model Selection and Multimodel Inference in Behavioral Ecology: Some Background, Observations, and Comparisons.” Behavioral Ecology and Sociobiology 65: 23–35.
Campagna, S., B. Lévesque, E. Anassour Laouan‐Sidi, et al. 2011. “Seroprevalence of 10 Zoonotic Infections in 2 Canadian Cree Communities.” Diagnostic Microbiology and Infectious Disease 70: 191–199.
Di Guardo, G., A. Di Cesare, D. Otranto, et al. 2011. “Genotyping of Toxoplasma gondii Isolates in Meningo‐Encephalitis Affected Striped Dolphins (Stenella coeruleoalba) from Italy.” Veterinary Parasitology 183: 31–36.
Dormann, C. F., J. M. Calabrese, G. Guillera‐Arroita, et al. 2018. “Model Averaging in Ecology: A Review of Bayesian, Information‐Theoretic, and Tactical Approaches for Predictive Inference.” Ecology Monographs 88: 485–504.
Dubey, J. P. 2010. Toxoplasmosis of Animals and Humans. 2nd ed, 1–313. Boca Raton, FL: CRC.
Dubey, J. P., F. H. A. Murata, C. K. Cerqueira‐Cézar, O. C. H. Kwok, and M. E. Grigg. 2020. “Recent Epidemiologic and Clinical Importance of Toxoplasma gondii Infections in Marine Mammals: 2009–2020.” Veterinary Parasitology 288: 109296.
Dubey, J. P., F. H. A. Murata, C. K. Cerqueira‐Cézar, O. C. H. Kwok, and I. Villena. 2021. “Congenital Toxoplasmosis in Humans: An Update of Worldwide Rate of Congenital Infections.” Parasitology 148: 1406–1416.
Ducrocq, J., B. Lévesque, M. Lemire, and G. de Serres. 2021. Zoonotic and Gastrointestinal Diseases. Nunavik Inuit Health Survey 2017 Qanuilirpitaa? How Are We Now? Quebec: Nunavik Regional Board of Health and Social Services (NRBHSS) & Institut National de Santé Publique du Québec (INSPQ).
Ducrocq, J., M. Ndao, C. P. Yansouni, et al. 2021. “Epidemiology Associated With the Exposure to Toxoplasma gondii in Nunavik's Inuit Population Using the 2017 Qanuilirpitaa Cross‐Sectional Health Survey.” Zoonoses and Public Health 68: 803–814.
Egeland, G. M. 2010a. Inuit Health Survey 2007–2008: Nunavut. Ste‐Anne‐de‐Bellevue, QC: Centre for Indigenous Peoples' Nutrition and Environment. McGill University.
Egeland, G. M. 2010b. Inuit Health Survey 2007–2008: Nunatsiavut. Ste‐Anne‐de‐Bellevue, QC: Centre for Indigenous Peoples' Nutrition and Environment. McGill University.
Fagerland, M. W., D. W. Hosmer, and A. M. Bofin. 2008. “Multinomial Goodness‐of‐Fit Tests for Logistic Regression Models.” Statistics in Medicine 27: 4238–4253.
Grigg, M. E., and J. C. Boothroyd. 2001. “Rapid Identification of Virulent Type I Strains of the Protozoan Pathogen Toxoplasma gondii by PCR‐Restriction Fragment Length Polymorphism Analysis at the B1 Gene.” Journal of Clinical Microbiology 39, no. 1: 398–400. https://doi.org/10.1128/JCM.39.1.398‐400.
Hall, T. A. 1999. “BioEdit: A User‐Friendly Biological Sequence Alignment Editor and Analysis Program for Windows 95/98/NT.” Nucleic Acids Symposium Series 41: 95–98.
Harris, L., J.‐S. Moore, K. Dunmall, et al. 2022. “Arctic Char in a Rapidly Changing North.” Polar Knowledge: Aqhaliat Report 4: 34–57. https://doi.org/10.35298/pkc.2021.02.eng.
Jenkins, E. J., L. J. Castrodale, S. J. C. de Rosemond, et al. 2013. “Chapter Two—Tradition and Transition: Parasitic Zoonoses of People and Animals in Alaska, Northern Canada, and Greenland.” Advances in Parasitology 82: 33–204.
Lindsay, D. S., and J. P. Dubey. 2009. “Long‐Term Survival of Toxoplasma gondii Sporulated Oocysts in Seawater.” Journal of Parasitology 95: 1019–1020.
Mainguy, J., A. Arsenault, L. Tran, et al. 2023b. “Otolith‐Inferred Patterns of Marine Migration Frequency in Nunavik Arctic Charr.” Journal of Fish Biology 103: 884–896.
Mainguy, J., and L. Beaupré. 2021. “Establishing a Benchmark Population Status for Arctic Char in the Five Mile Inlet system, Inukjuak, 2018”. Ministère des Forêts, de la Faune et des Parcs, Direction de l'expertise sur la Faune Aquatique et Direction de la Gestion de la Faune du Nord‐du‐Québec, p. 32. https://mffp.gouv.qc.ca/documents/wildlife/RE_Inukjuak_%20Arctic_Char.pdf.
Mainguy, J., L. Beaupré, and V. Nadeau. 2023a. “Establishment of a Reference State for the Tasiallujuak River Arctic Charr Population, Salluit, Summer 2019”. Ministère de l'Environnement, de la Lutte Contre les Changements Climatiques, de la Faune et des Parcs. Direction de l'Expertise sur la Faune Aquatique and Direction de la Gestion de la Faune du Nord‐du‐Québec, p. 37. https://mffp.gouv.qc.ca/documents/wildlife/report‐salluit‐arctic‐charr.pdf.
Marino, A. M. F., R. P. Giunta, A. Salvaggio, et al. 2019. “Toxoplasma gondii in Edible Fishes Captured in the Mediterranean Basin.” Zoonoses and Public Health 66: 826–834.
Massie, G. N., M. W. Ware, E. N. Villegas, and M. W. Black. 2010. “Uptake and Transmission of Toxoplasma gondii Oocysts by Migratory, Filter‐Feeding Fish.” Veterinary Parasitology 169: 296–303.
Merks, H., R. Boone, N. Janecko, M. Viswanathan, and B. R. Dixon. 2023. “Foodborne Protozoan Parasites in Fresh Mussels and Oysters Purchased at Retail in Canada.” International Journal of Food Microbiology 399: 110248.
Messier, V., B. Lévesque, J. F. Proulx, et al. 2009. “Seroprevalence of Toxoplasma gondii Among Nunavik Inuit (Canada).” Zoonoses and Public Health 56: 188–197.
Murdoch, A., J. B. Dempson, F. Martin, and M. Power. 2015. “Temperature‐Growth Patterns of Individually Tagged Anadromous Arctic Charr Salvelinus alpinus in Ungava and Labrador, Canada.” Ecology of Freshwater Fish 24: 193–203.
Neumann, M. 2021. “MNLpred—Simulated Predicted Probabilities for Multinomial Logit Models (Version 0.0.8)”. https://CRAN.R‐project.org/package=MNLpred.
Nichols, R. A. B., B. M. Campbell, and H. V. Smith. 2003. “Identification of Cryptosporidium spp. Oocysts in United Kingdom Noncarbonated Natural Mineral Waters and Drinking Waters by Using a Modified Nested PCR‐Restriction Fragment Length Polymorphism Assay.” Applied and Environmental Microbiology 69: 4183–4189.
Nunavik Food Guide Educator's Handbook. n.d. “Nunavik Regional Board of Health and Social Services”. Accessed July 6, 2013. https://nrbhss.ca/en/nrbhss/public‐health/prevention‐and‐health‐promotion/healthy‐eating.
Omata, Y., Y. Umeshita, T. Murao, et al. 2005. “Toxoplasma gondii Does Not Persist in Goldfish (Carassius auratus).” Journal of Parasitology 91: 1496–1499.
R Core Team. 2023. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.
Reiling, S. J., and B. R. Dixon. 2019. “Toxoplasma gondii: How an Amazonian Parasite Became an Inuit Health Issue.” Canada Communicable Disease Report 45: 183–190.
Reiling, S. J., L. Measures, S. Feng, R. Boone, H. Merks, and B. R. Dixon. 2019. “Toxoplasma gondii, Sarcocystis sp. and Neospora caninum‐Like Parasites in Seals From Northern and Eastern Canada: Potential Risk to Consumers.” Food and Waterborne Parasitology 17: e00067.
Sanders, J. L., Y. Zhou, H. M. Moulton, et al. 2015. “The Zebrafish, Danio rerio, as a Model for Toxoplasma gondii: An Initial Description of Infection in Fish.” Journal of Fish Diseases 38: 675–679.
Shapiro, K., L. Bahia‐Oliveira, B. Dixon, et al. 2019. “Environmental Transmission of Toxoplasma gondii: Oocysts in Water, Soil and Food.” Food and Waterborne Parasitology 15: e00049.
Simon, A., M. Bigras Poulin, A. N. Rousseau, J. P. Dubey, and N. H. Ogden. 2013a. “Spatiotemporal Dynamics of Toxoplasma gondii Infection in Canadian Lynx (Lynx canadensis) in Western Québec, Canada.” Journal of Wildlife Diseases 49: 39–48.
Simon, A., M. B. Poulin, A. N. Rousseau, and N. H. Ogden. 2013b. “Fate and Transport of Toxoplasma gondii Oocysts in Seasonally Snow Covered Watersheds: A Conceptual Framework From a Melting Snowpack to the Canadian Arctic Coasts.” International Journal of Environmental Research and Public Health 10: 994–1005.
Statistics Canada. 2010. Human Activity and the Environment. Section 2: Canada's Water Supply—Stocks and Flows. Ottawa, ON: Statistics Canada.
Stewart, D. B., and K. L. Howland. 2009. An Ecological and Oceanographical Assessment of the Alternate Ballast Water Exchange Zone in the Hudson Strait Region (Canadian Science Advisory Secretariat). Winnipeg, MB: Fisheries and Oceans Canada.
Taghadosi, C., G. A. Kojouri, and M. A. Taheri. 2010. “Detection of Toxoplasma Antibodies in Sera of Salmonidae by ELISA.” Comparative Clinical Pathology 19: 203–206.
Venables, W. N., and B. D. Ripley. 2002. Modern Applied Statistics With S. 4th ed. New York, NY: Springer.
Willis, J. E., J. T. McClure, J. Davidson, C. McClure, and S. J. Greenwood. 2013. “Global Occurrence of Cryptosporidium and Giardia in Shellfish: Should Canada Take a Closer Look?” Food Research International 52: 119–135.
Yang, Y., S. M. Yu, K. Chen, G. Hide, Z. R. Lun, and D. H. Lai. 2020. “Temperature Is a Key Factor Influencing the Invasion and Proliferation of Toxoplasma gondii in Fish Cells.” Experimental Parasitology 217: 107966.
Zhang, M., Z. Yang, S. Wang, et al. 2014. “Detection of Toxoplasma gondii in Shellfish and Fish in Parts of China.” Veterinary Parasitology 200: 85–89.