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Environmental reservoir dynamics predict global infection patterns and population impacts for the fungal disease white-nose syndrome

Disease outbreaks and pathogen introductions can have significant effects on host populations, and the ability of pathogens to persist in the environment can exacerbate disease impacts by fueling sustained transmission, seasonal epidemics, and repeated spillover events. While theory suggests that th...

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Autores principales: Hoyt, Joseph R., Langwig, Kate E., Sun, Keping, Parise, Katy L., Li, Aoqiang, Wang, Yujuan, Huang, Xiaobin, Worledge, Lisa, Miller, Helen, White, J. Paul, Kaarakka, Heather M., Redell, Jennifer A., Görföl, Tamás, Boldogh, Sándor András, Fukui, Dai, Sakuyama, Muneki, Yachimori, Syuuji, Sato, Akiyoshi, Dalannast, Munkhnast, Jargalsaikhan, Ariunbold, Batbayar, Nyambayar, Yovel, Yossi, Amichai, Eran, Natradze, Ioseb, Frick, Winifred F., Foster, Jeffrey T., Feng, Jiang, Kilpatrick, A. Marm
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7132137/
https://www.ncbi.nlm.nih.gov/pubmed/32179668
http://dx.doi.org/10.1073/pnas.1914794117
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author Hoyt, Joseph R.
Langwig, Kate E.
Sun, Keping
Parise, Katy L.
Li, Aoqiang
Wang, Yujuan
Huang, Xiaobin
Worledge, Lisa
Miller, Helen
White, J. Paul
Kaarakka, Heather M.
Redell, Jennifer A.
Görföl, Tamás
Boldogh, Sándor András
Fukui, Dai
Sakuyama, Muneki
Yachimori, Syuuji
Sato, Akiyoshi
Dalannast, Munkhnast
Jargalsaikhan, Ariunbold
Batbayar, Nyambayar
Yovel, Yossi
Amichai, Eran
Natradze, Ioseb
Frick, Winifred F.
Foster, Jeffrey T.
Feng, Jiang
Kilpatrick, A. Marm
author_facet Hoyt, Joseph R.
Langwig, Kate E.
Sun, Keping
Parise, Katy L.
Li, Aoqiang
Wang, Yujuan
Huang, Xiaobin
Worledge, Lisa
Miller, Helen
White, J. Paul
Kaarakka, Heather M.
Redell, Jennifer A.
Görföl, Tamás
Boldogh, Sándor András
Fukui, Dai
Sakuyama, Muneki
Yachimori, Syuuji
Sato, Akiyoshi
Dalannast, Munkhnast
Jargalsaikhan, Ariunbold
Batbayar, Nyambayar
Yovel, Yossi
Amichai, Eran
Natradze, Ioseb
Frick, Winifred F.
Foster, Jeffrey T.
Feng, Jiang
Kilpatrick, A. Marm
author_sort Hoyt, Joseph R.
collection PubMed
description Disease outbreaks and pathogen introductions can have significant effects on host populations, and the ability of pathogens to persist in the environment can exacerbate disease impacts by fueling sustained transmission, seasonal epidemics, and repeated spillover events. While theory suggests that the presence of an environmental reservoir increases the risk of host declines and threat of extinction, the influence of reservoir dynamics on transmission and population impacts remains poorly described. Here we show that the extent of the environmental reservoir explains broad patterns of host infection and the severity of disease impacts of a virulent pathogen. We examined reservoir and host infection dynamics and the resulting impacts of Pseudogymnoascus destructans, the fungal pathogen that causes white-nose syndrome, in 39 species of bats at 101 sites across the globe. Lower levels of pathogen in the environment consistently corresponded to delayed infection of hosts, fewer and less severe infections, and reduced population impacts. In contrast, an extensive and persistent environmental reservoir led to early and widespread infections and severe population declines. These results suggest that continental differences in the persistence or decay of P. destructans in the environment altered infection patterns in bats and influenced whether host populations were stable or experienced severe declines from this disease. Quantifying the impact of the environmental reservoir on disease dynamics can provide specific targets for reducing pathogen levels in the environment to prevent or control future epidemics.
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spelling pubmed-71321372020-04-09 Environmental reservoir dynamics predict global infection patterns and population impacts for the fungal disease white-nose syndrome Hoyt, Joseph R. Langwig, Kate E. Sun, Keping Parise, Katy L. Li, Aoqiang Wang, Yujuan Huang, Xiaobin Worledge, Lisa Miller, Helen White, J. Paul Kaarakka, Heather M. Redell, Jennifer A. Görföl, Tamás Boldogh, Sándor András Fukui, Dai Sakuyama, Muneki Yachimori, Syuuji Sato, Akiyoshi Dalannast, Munkhnast Jargalsaikhan, Ariunbold Batbayar, Nyambayar Yovel, Yossi Amichai, Eran Natradze, Ioseb Frick, Winifred F. Foster, Jeffrey T. Feng, Jiang Kilpatrick, A. Marm Proc Natl Acad Sci U S A Biological Sciences Disease outbreaks and pathogen introductions can have significant effects on host populations, and the ability of pathogens to persist in the environment can exacerbate disease impacts by fueling sustained transmission, seasonal epidemics, and repeated spillover events. While theory suggests that the presence of an environmental reservoir increases the risk of host declines and threat of extinction, the influence of reservoir dynamics on transmission and population impacts remains poorly described. Here we show that the extent of the environmental reservoir explains broad patterns of host infection and the severity of disease impacts of a virulent pathogen. We examined reservoir and host infection dynamics and the resulting impacts of Pseudogymnoascus destructans, the fungal pathogen that causes white-nose syndrome, in 39 species of bats at 101 sites across the globe. Lower levels of pathogen in the environment consistently corresponded to delayed infection of hosts, fewer and less severe infections, and reduced population impacts. In contrast, an extensive and persistent environmental reservoir led to early and widespread infections and severe population declines. These results suggest that continental differences in the persistence or decay of P. destructans in the environment altered infection patterns in bats and influenced whether host populations were stable or experienced severe declines from this disease. Quantifying the impact of the environmental reservoir on disease dynamics can provide specific targets for reducing pathogen levels in the environment to prevent or control future epidemics. National Academy of Sciences 2020-03-31 2020-03-16 /pmc/articles/PMC7132137/ /pubmed/32179668 http://dx.doi.org/10.1073/pnas.1914794117 Text en Copyright © 2020 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/ https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Hoyt, Joseph R.
Langwig, Kate E.
Sun, Keping
Parise, Katy L.
Li, Aoqiang
Wang, Yujuan
Huang, Xiaobin
Worledge, Lisa
Miller, Helen
White, J. Paul
Kaarakka, Heather M.
Redell, Jennifer A.
Görföl, Tamás
Boldogh, Sándor András
Fukui, Dai
Sakuyama, Muneki
Yachimori, Syuuji
Sato, Akiyoshi
Dalannast, Munkhnast
Jargalsaikhan, Ariunbold
Batbayar, Nyambayar
Yovel, Yossi
Amichai, Eran
Natradze, Ioseb
Frick, Winifred F.
Foster, Jeffrey T.
Feng, Jiang
Kilpatrick, A. Marm
Environmental reservoir dynamics predict global infection patterns and population impacts for the fungal disease white-nose syndrome
title Environmental reservoir dynamics predict global infection patterns and population impacts for the fungal disease white-nose syndrome
title_full Environmental reservoir dynamics predict global infection patterns and population impacts for the fungal disease white-nose syndrome
title_fullStr Environmental reservoir dynamics predict global infection patterns and population impacts for the fungal disease white-nose syndrome
title_full_unstemmed Environmental reservoir dynamics predict global infection patterns and population impacts for the fungal disease white-nose syndrome
title_short Environmental reservoir dynamics predict global infection patterns and population impacts for the fungal disease white-nose syndrome
title_sort environmental reservoir dynamics predict global infection patterns and population impacts for the fungal disease white-nose syndrome
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7132137/
https://www.ncbi.nlm.nih.gov/pubmed/32179668
http://dx.doi.org/10.1073/pnas.1914794117
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