Modeling the Transmission of Vibrio aestuarianus in Pacific Oysters Using Experimental Infection Data

Vibrio aestuarianus is a bacterium related to mortality outbreaks in Pacific oysters, Crassostrea gigas, in France, Ireland, and Scotland since 2011. Knowledge about its transmission dynamics is still lacking, impairing guidance to prevent and control the related disease spread. Mathematical modelin...

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Published in:Frontiers in Veterinary Science
Main Authors: Lupo, Coralie, Travers, Marie-agnes, Tourbiez, Delphine, Barthélémy, Clement, Beaunée, Gaël, Ezanno, Pauline
Format: Article in Journal/Newspaper
Language:English
Published: Frontiers Media SA 2019
Subjects:
Online Access:https://archimer.ifremer.fr/doc/00495/60652/64148.pdf
https://archimer.ifremer.fr/doc/00495/60652/64149.pdf
https://doi.org/10.3389/fvets.2019.00142
https://archimer.ifremer.fr/doc/00495/60652/
id ftarchimer:oai:archimer.ifremer.fr:60652
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spelling ftarchimer:oai:archimer.ifremer.fr:60652 2023-05-15T15:58:26+02:00 Modeling the Transmission of Vibrio aestuarianus in Pacific Oysters Using Experimental Infection Data Lupo, Coralie Travers, Marie-agnes Tourbiez, Delphine Barthélémy, Clement Beaunée, Gaël Ezanno, Pauline 2019-05 application/pdf https://archimer.ifremer.fr/doc/00495/60652/64148.pdf https://archimer.ifremer.fr/doc/00495/60652/64149.pdf https://doi.org/10.3389/fvets.2019.00142 https://archimer.ifremer.fr/doc/00495/60652/ eng eng Frontiers Media SA https://archimer.ifremer.fr/doc/00495/60652/64148.pdf https://archimer.ifremer.fr/doc/00495/60652/64149.pdf doi:10.3389/fvets.2019.00142 https://archimer.ifremer.fr/doc/00495/60652/ info:eu-repo/semantics/openAccess restricted use Frontiers In Veterinary Science (2297-1769) (Frontiers Media SA), 2019-05 , Vol. 6 , N. 142 , P. 15p. marine epidemiology parameter estimation compartmental model ABC method global sensitivity analysis basic reproduction number R-0 Crassostrea gigas oyster mortality text Publication info:eu-repo/semantics/article 2019 ftarchimer https://doi.org/10.3389/fvets.2019.00142 2021-09-23T20:32:41Z Vibrio aestuarianus is a bacterium related to mortality outbreaks in Pacific oysters, Crassostrea gigas, in France, Ireland, and Scotland since 2011. Knowledge about its transmission dynamics is still lacking, impairing guidance to prevent and control the related disease spread. Mathematical modeling is a relevant approach to better understand the determinants of a disease and predict its dynamics in imperfectly observed pathosystems. We developed here the first marine epidemiological model to estimate the key parameters of V. aestuarianus infection at a local scale in a small and closed oyster population under controlled laboratory conditions. Using a compartmental model accounting for free-living bacteria in seawater, we predicted the infection dynamics using dedicated and model-driven collected laboratory experimental transmission data. We estimated parameters and showed that waterborne transmission of V. aestuarianus is possible under experimental conditions, with a basic reproduction number R0 of 2.88 (95% CI: 1.86; 3.35), and a generation time of 5.5 days. Our results highlighted a bacterial dose–dependent transmission of vibriosis at local scale. Global sensitivity analyses indicated that the bacteria shedding rate, the concentration of bacteria in seawater that yields a 50% chance of catching the infection, and the initial bacterial exposure dose W0 were three critical parameters explaining most of the variation in the selected model outputs related to disease spread, i.e., R0, the maximum prevalence, oyster survival curve, and bacteria concentration in seawater. Prevention and control should target the exposure of oysters to bacterial concentration in seawater. This combined laboratory–modeling approach enabled us to maximize the use of information obtained through experiments. The identified key epidemiological parameters should be better refined by further dedicated laboratory experiments. These results revealed the importance of multidisciplinary approaches to gain consistent insights into the marine epidemiology of oyster diseases. Article in Journal/Newspaper Crassostrea gigas Archimer (Archive Institutionnelle de l'Ifremer - Institut français de recherche pour l'exploitation de la mer) Pacific Frontiers in Veterinary Science 6
institution Open Polar
collection Archimer (Archive Institutionnelle de l'Ifremer - Institut français de recherche pour l'exploitation de la mer)
op_collection_id ftarchimer
language English
topic marine epidemiology
parameter estimation
compartmental model
ABC method
global sensitivity analysis
basic reproduction number R-0
Crassostrea gigas
oyster mortality
spellingShingle marine epidemiology
parameter estimation
compartmental model
ABC method
global sensitivity analysis
basic reproduction number R-0
Crassostrea gigas
oyster mortality
Lupo, Coralie
Travers, Marie-agnes
Tourbiez, Delphine
Barthélémy, Clement
Beaunée, Gaël
Ezanno, Pauline
Modeling the Transmission of Vibrio aestuarianus in Pacific Oysters Using Experimental Infection Data
topic_facet marine epidemiology
parameter estimation
compartmental model
ABC method
global sensitivity analysis
basic reproduction number R-0
Crassostrea gigas
oyster mortality
description Vibrio aestuarianus is a bacterium related to mortality outbreaks in Pacific oysters, Crassostrea gigas, in France, Ireland, and Scotland since 2011. Knowledge about its transmission dynamics is still lacking, impairing guidance to prevent and control the related disease spread. Mathematical modeling is a relevant approach to better understand the determinants of a disease and predict its dynamics in imperfectly observed pathosystems. We developed here the first marine epidemiological model to estimate the key parameters of V. aestuarianus infection at a local scale in a small and closed oyster population under controlled laboratory conditions. Using a compartmental model accounting for free-living bacteria in seawater, we predicted the infection dynamics using dedicated and model-driven collected laboratory experimental transmission data. We estimated parameters and showed that waterborne transmission of V. aestuarianus is possible under experimental conditions, with a basic reproduction number R0 of 2.88 (95% CI: 1.86; 3.35), and a generation time of 5.5 days. Our results highlighted a bacterial dose–dependent transmission of vibriosis at local scale. Global sensitivity analyses indicated that the bacteria shedding rate, the concentration of bacteria in seawater that yields a 50% chance of catching the infection, and the initial bacterial exposure dose W0 were three critical parameters explaining most of the variation in the selected model outputs related to disease spread, i.e., R0, the maximum prevalence, oyster survival curve, and bacteria concentration in seawater. Prevention and control should target the exposure of oysters to bacterial concentration in seawater. This combined laboratory–modeling approach enabled us to maximize the use of information obtained through experiments. The identified key epidemiological parameters should be better refined by further dedicated laboratory experiments. These results revealed the importance of multidisciplinary approaches to gain consistent insights into the marine epidemiology of oyster diseases.
format Article in Journal/Newspaper
author Lupo, Coralie
Travers, Marie-agnes
Tourbiez, Delphine
Barthélémy, Clement
Beaunée, Gaël
Ezanno, Pauline
author_facet Lupo, Coralie
Travers, Marie-agnes
Tourbiez, Delphine
Barthélémy, Clement
Beaunée, Gaël
Ezanno, Pauline
author_sort Lupo, Coralie
title Modeling the Transmission of Vibrio aestuarianus in Pacific Oysters Using Experimental Infection Data
title_short Modeling the Transmission of Vibrio aestuarianus in Pacific Oysters Using Experimental Infection Data
title_full Modeling the Transmission of Vibrio aestuarianus in Pacific Oysters Using Experimental Infection Data
title_fullStr Modeling the Transmission of Vibrio aestuarianus in Pacific Oysters Using Experimental Infection Data
title_full_unstemmed Modeling the Transmission of Vibrio aestuarianus in Pacific Oysters Using Experimental Infection Data
title_sort modeling the transmission of vibrio aestuarianus in pacific oysters using experimental infection data
publisher Frontiers Media SA
publishDate 2019
url https://archimer.ifremer.fr/doc/00495/60652/64148.pdf
https://archimer.ifremer.fr/doc/00495/60652/64149.pdf
https://doi.org/10.3389/fvets.2019.00142
https://archimer.ifremer.fr/doc/00495/60652/
geographic Pacific
geographic_facet Pacific
genre Crassostrea gigas
genre_facet Crassostrea gigas
op_source Frontiers In Veterinary Science (2297-1769) (Frontiers Media SA), 2019-05 , Vol. 6 , N. 142 , P. 15p.
op_relation https://archimer.ifremer.fr/doc/00495/60652/64148.pdf
https://archimer.ifremer.fr/doc/00495/60652/64149.pdf
doi:10.3389/fvets.2019.00142
https://archimer.ifremer.fr/doc/00495/60652/
op_rights info:eu-repo/semantics/openAccess
restricted use
op_doi https://doi.org/10.3389/fvets.2019.00142
container_title Frontiers in Veterinary Science
container_volume 6
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