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      Are foxes ( Vulpes spp.) good sentinel species for Toxoplasma gondii in northern Canada?

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          Abstract

          Background

          In changing northern ecosystems, understanding the mechanisms of transmission of zoonotic pathogens, including the coccidian parasite Toxoplasma gondii, is essential to protect the health of vulnerable animals and humans. As high-level predators and scavengers, foxes represent a potentially sensitive indicator of the circulation of T. gondii in environments where humans co-exist. The objectives of our research were to compare serological and molecular assays to detect T. gondii, generate baseline data on T. gondii antibody and tissue prevalence in foxes in northern Canada, and compare regional seroprevalence in foxes with that in people from recently published surveys across northern Canada.

          Methods

          Fox carcasses ( Vulpes vulpes/ Vulpes lagopus, n = 749) were collected by local trappers from the eastern (Labrador and Québec) and western Canadian Arctic (northern Manitoba, Nunavut, and the Northwest Territories) during the winters of 2015–2019. Antibodies in heart fluid were detected using a commercial enzyme-linked immunosorbent assay. Toxoplasma gondii DNA was detected in hearts and brains using a magnetic capture DNA extraction and real-time PCR assay.

          Results

          Antibodies against T. gondii and DNA were detected in 36% and 27% of foxes, respectively. Detection of antibodies was higher in older (64%) compared to younger foxes (22%). More males (36%) than females (31%) were positive for antibodies to T. gondii. Tissue prevalence in foxes from western Nunavik (51%) was higher than in eastern Nunavik (19%). At the Canadian scale, T. gondii exposure was lower in western Inuit regions (13%) compared to eastern Inuit regions (39%), possibly because of regional differences in fox diet and/or environment. Exposure to T. gondii decreased at higher latitude and in foxes having moderate to little fat. Higher mean infection intensity was observed in Arctic foxes compared to red foxes. Fox and human seroprevalence showed similar trends across Inuit regions of Canada, but were less correlated in the eastern sub-Arctic, which may reflect regional differences in human dietary preferences.

          Conclusions

          Our study sheds new light on the current status of T. gondii in foxes in northern Canada and shows that foxes serve as a good sentinel species for environmental circulation and, in some regions, human exposure to this parasite in the Arctic.

          Graphical Abstract

          Supplementary Information

          The online version contains supplementary material available at 10.1186/s13071-022-05229-3.

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          Most cited references68

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          Fitting Linear Mixed-Effects Models Usinglme4

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            Fitting Linear Mixed-Effects Models Using lme4

            Maximum likelihood or restricted maximum likelihood (REML) estimates of the parameters in linear mixed-effects models can be determined using the lmer function in the lme4 package for R. As for most model-fitting functions in R, the model is described in an lmer call by a formula, in this case including both fixed- and random-effects terms. The formula and data together determine a numerical representation of the model from which the profiled deviance or the profiled REML criterion can be evaluated as a function of some of the model parameters. The appropriate criterion is optimized, using one of the constrained optimization functions in R, to provide the parameter estimates. We describe the structure of the model, the steps in evaluating the profiled deviance or REML criterion, and the structure of classes or types that represents such a model. Sufficient detail is included to allow specialization of these structures by users who wish to write functions to fit specialized linear mixed models, such as models incorporating pedigrees or smoothing splines, that are not easily expressible in the formula language used by lmer. Journal of Statistical Software, 67 (1) ISSN:1548-7660
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              A protocol for data exploration to avoid common statistical problems

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                Author and article information

                Contributors
                emb232@mail.usask.ca
                rajgangahar@gmail.com
                adrian_hoz@hotmail.com
                kaylabuhler_1@hotmail.com
                batol.al-adhami@inspection.gc.ca
                csu1@utk.edu
                hmafenton@gmail.com
                ggouin@makivik.org
                jim.roth@umanitoba.ca
                warretrc@myumanitoba.ca
                carla.pamak@nunatsiavut.com
                audrey.simon@umontreal.ca
                nickbachand@gmail.com
                patrick.a.leighton@umontreal.ca
                emily.jenkins@usask.ca
                Journal
                Parasit Vectors
                Parasit Vectors
                Parasites & Vectors
                BioMed Central (London )
                1756-3305
                1 April 2022
                1 April 2022
                2022
                : 15
                : 115
                Affiliations
                [1 ]GRID grid.25152.31, ISNI 0000 0001 2154 235X, Department of Veterinary Microbiology, , University of Saskatchewan, ; Saskatoon, SK Canada
                [2 ]Centre for Food-Borne and Animal Parasitology, Saskatoon, SK Canada
                [3 ]GRID grid.411461.7, ISNI 0000 0001 2315 1184, Department of Microbiology, , University of Tennessee, ; Knoxville, TN USA
                [4 ]GRID grid.412247.6, ISNI 0000 0004 1776 0209, Ross University School of Veterinary Medicine, ; Basseterre, Saint Kitts and Nevis
                [5 ]GRID grid.55614.33, ISNI 0000 0001 1302 4958, Nunavik Research Centre, ; Kuujjuaq, QC Canada
                [6 ]GRID grid.21613.37, ISNI 0000 0004 1936 9609, Department of Biological Sciences, , University of Manitoba, ; Winnipeg, MB Canada
                [7 ]GRID grid.55614.33, ISNI 0000 0001 1302 4958, Nunatsiavut Research Centre, ; Nain, NL Canada
                [8 ]GRID grid.14848.31, ISNI 0000 0001 2292 3357, Research Group On Epidemiology of Zoonoses and Public Health (GREZOSP), , Université de Montréal, ; Saint-Hyacinthe, QC Canada
                Author information
                http://orcid.org/0000-0002-2430-9083
                Article
                5229
                10.1186/s13071-022-05229-3
                8972674
                35365191
                cc8105e2-01f6-425a-88f4-ff075a4206d1
                © The Author(s) 2022

                Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

                History
                : 14 January 2022
                : 2 March 2022
                Funding
                Funded by: ArcticNet Networks of Centres of Excellence
                Funded by: FundRef http://dx.doi.org/10.13039/501100000038, Natural Sciences and Engineering Research Council of Canada;
                Funded by: FundRef http://dx.doi.org/10.13039/100012258, Polar Knowledge Canada;
                Funded by: Weston Family Foundation
                Funded by: US National Center for Veterinary Parasitology
                Categories
                Research
                Custom metadata
                © The Author(s) 2022

                Parasitology
                toxoplasma gondii,elisa,mc-qpcr,foxes,sentinel species,canada
                Parasitology
                toxoplasma gondii, elisa, mc-qpcr, foxes, sentinel species, canada

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