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Novel insights into serodiagnosis and epidemiology of Erysipelothrix rhusiopathiae, a newly recognized pathogen in muskoxen (Ovibos moschatus)

BACKGROUND: Muskoxen are a key species of Arctic ecosystems and are important for food security and socio-economic well-being of many Indigenous communities in the Arctic and Subarctic. Between 2009 and 2014, the bacterium Erysipelothrix rhusiopathiae was isolated for the first time in this species...

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Autores principales: Mavrot, Fabien, Orsel, Karin, Hutchins, Wendy, Adams, Layne G., Beckmen, Kimberlee, Blake, John E., Checkley, Sylvia L., Davison, Tracy, Di Francesco, Juliette, Elkin, Brett, Leclerc, Lisa-Marie, Schneider, Angela, Tomaselli, Matilde, Kutz, Susan J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7173868/
https://www.ncbi.nlm.nih.gov/pubmed/32315366
http://dx.doi.org/10.1371/journal.pone.0231724
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author Mavrot, Fabien
Orsel, Karin
Hutchins, Wendy
Adams, Layne G.
Beckmen, Kimberlee
Blake, John E.
Checkley, Sylvia L.
Davison, Tracy
Di Francesco, Juliette
Elkin, Brett
Leclerc, Lisa-Marie
Schneider, Angela
Tomaselli, Matilde
Kutz, Susan J.
author_facet Mavrot, Fabien
Orsel, Karin
Hutchins, Wendy
Adams, Layne G.
Beckmen, Kimberlee
Blake, John E.
Checkley, Sylvia L.
Davison, Tracy
Di Francesco, Juliette
Elkin, Brett
Leclerc, Lisa-Marie
Schneider, Angela
Tomaselli, Matilde
Kutz, Susan J.
author_sort Mavrot, Fabien
collection PubMed
description BACKGROUND: Muskoxen are a key species of Arctic ecosystems and are important for food security and socio-economic well-being of many Indigenous communities in the Arctic and Subarctic. Between 2009 and 2014, the bacterium Erysipelothrix rhusiopathiae was isolated for the first time in this species in association with multiple mortality events in Canada and Alaska, raising questions regarding the spatiotemporal occurrence of the pathogen and its potential impact on muskox populations. MATERIALS AND METHODS: We adapted a commercial porcine E. rhusiopathiae enzyme-linked immunosorbent assay to test 958 blood samples that were collected from muskoxen from seven regions in Alaska and the Canadian Arctic between 1976 and 2017. The cut-off between negative and positive results was established using mixture-distribution analysis, a data-driven approach. Based on 818 samples for which a serological status could be determined and with complete information, we calculated trends in sample seroprevalences in population time-series and compared them with population trends in the investigated regions. RESULTS: Overall, 219/818 (27.8%, 95% Confidence Interval: 24.7–31.0) samples were classified as positive for exposure to E. rhusiopathiae. There were large variations between years and regions. Seropositive animals were found among the earliest serum samples tested; 1976 in Alaska and 1991 in Canada. In Alaskan muskoxen, sample seroprevalence increased after 2000 and, in two regions, peak seroprevalences occurred simultaneously with population declines. In one of these regions, concurrent unusual mortalities were observed and E. rhusiopathiae was isolated from muskox carcasses. In Canada, there was an increase in sample seroprevalence in two muskox populations following known mortality events that had been attributed to E. rhusiopathiae. CONCLUSION: Our results indicate widespread exposure of muskoxen to E. rhusiopathiae in western Canada and Alaska. Although not new to the Arctic, we documented an increased exposure to the pathogen in several regions concurrent with population declines. Understanding causes for the apparent increased occurrence of this pathogen and its association with large scale mortality events for muskoxen is critical to evaluate the implications for wildlife and wildlife-dependent human populations in the Arctic.
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spelling pubmed-71738682020-04-27 Novel insights into serodiagnosis and epidemiology of Erysipelothrix rhusiopathiae, a newly recognized pathogen in muskoxen (Ovibos moschatus) Mavrot, Fabien Orsel, Karin Hutchins, Wendy Adams, Layne G. Beckmen, Kimberlee Blake, John E. Checkley, Sylvia L. Davison, Tracy Di Francesco, Juliette Elkin, Brett Leclerc, Lisa-Marie Schneider, Angela Tomaselli, Matilde Kutz, Susan J. PLoS One Research Article BACKGROUND: Muskoxen are a key species of Arctic ecosystems and are important for food security and socio-economic well-being of many Indigenous communities in the Arctic and Subarctic. Between 2009 and 2014, the bacterium Erysipelothrix rhusiopathiae was isolated for the first time in this species in association with multiple mortality events in Canada and Alaska, raising questions regarding the spatiotemporal occurrence of the pathogen and its potential impact on muskox populations. MATERIALS AND METHODS: We adapted a commercial porcine E. rhusiopathiae enzyme-linked immunosorbent assay to test 958 blood samples that were collected from muskoxen from seven regions in Alaska and the Canadian Arctic between 1976 and 2017. The cut-off between negative and positive results was established using mixture-distribution analysis, a data-driven approach. Based on 818 samples for which a serological status could be determined and with complete information, we calculated trends in sample seroprevalences in population time-series and compared them with population trends in the investigated regions. RESULTS: Overall, 219/818 (27.8%, 95% Confidence Interval: 24.7–31.0) samples were classified as positive for exposure to E. rhusiopathiae. There were large variations between years and regions. Seropositive animals were found among the earliest serum samples tested; 1976 in Alaska and 1991 in Canada. In Alaskan muskoxen, sample seroprevalence increased after 2000 and, in two regions, peak seroprevalences occurred simultaneously with population declines. In one of these regions, concurrent unusual mortalities were observed and E. rhusiopathiae was isolated from muskox carcasses. In Canada, there was an increase in sample seroprevalence in two muskox populations following known mortality events that had been attributed to E. rhusiopathiae. CONCLUSION: Our results indicate widespread exposure of muskoxen to E. rhusiopathiae in western Canada and Alaska. Although not new to the Arctic, we documented an increased exposure to the pathogen in several regions concurrent with population declines. Understanding causes for the apparent increased occurrence of this pathogen and its association with large scale mortality events for muskoxen is critical to evaluate the implications for wildlife and wildlife-dependent human populations in the Arctic. Public Library of Science 2020-04-21 /pmc/articles/PMC7173868/ /pubmed/32315366 http://dx.doi.org/10.1371/journal.pone.0231724 Text en https://creativecommons.org/publicdomain/zero/1.0/ This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 (https://creativecommons.org/publicdomain/zero/1.0/) public domain dedication.
spellingShingle Research Article
Mavrot, Fabien
Orsel, Karin
Hutchins, Wendy
Adams, Layne G.
Beckmen, Kimberlee
Blake, John E.
Checkley, Sylvia L.
Davison, Tracy
Di Francesco, Juliette
Elkin, Brett
Leclerc, Lisa-Marie
Schneider, Angela
Tomaselli, Matilde
Kutz, Susan J.
Novel insights into serodiagnosis and epidemiology of Erysipelothrix rhusiopathiae, a newly recognized pathogen in muskoxen (Ovibos moschatus)
title Novel insights into serodiagnosis and epidemiology of Erysipelothrix rhusiopathiae, a newly recognized pathogen in muskoxen (Ovibos moschatus)
title_full Novel insights into serodiagnosis and epidemiology of Erysipelothrix rhusiopathiae, a newly recognized pathogen in muskoxen (Ovibos moschatus)
title_fullStr Novel insights into serodiagnosis and epidemiology of Erysipelothrix rhusiopathiae, a newly recognized pathogen in muskoxen (Ovibos moschatus)
title_full_unstemmed Novel insights into serodiagnosis and epidemiology of Erysipelothrix rhusiopathiae, a newly recognized pathogen in muskoxen (Ovibos moschatus)
title_short Novel insights into serodiagnosis and epidemiology of Erysipelothrix rhusiopathiae, a newly recognized pathogen in muskoxen (Ovibos moschatus)
title_sort novel insights into serodiagnosis and epidemiology of erysipelothrix rhusiopathiae, a newly recognized pathogen in muskoxen (ovibos moschatus)
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7173868/
https://www.ncbi.nlm.nih.gov/pubmed/32315366
http://dx.doi.org/10.1371/journal.pone.0231724
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