Phylodynamic analysis of the highly pathogenic avian influenza H5N8 epidemic in France, 2016–2017

In 2016–2017, France experienced a devastating epidemic of highly pathogenic avian influenza (HPAI) H5N8, with more than 400 outbreaks reported in poultry farms. We analyzed the spatiotemporal dynamics of the epidemic using a structured‐coalescent‐based phylodynamic approach that combined viral geno...

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Published inTransboundary and emerging diseases Vol. 69; no. 5; pp. e1574 - e1583
Main Authors Chakraborty, Debapriyo, Guinat, Claire, Müller, Nicola F., Briand, Francois‐Xavier, Andraud, Mathieu, Scoizec, Axelle, Lebouquin, Sophie, Niqueux, Eric, Schmitz, Audrey, Grasland, Beatrice, Guerin, Jean‐Luc, Paul, Mathilde C., Vergne, Timothée
Format Journal Article
LanguageEnglish
Published Germany John Wiley & Sons, Inc 01.09.2022
Wiley-Blackwell
John Wiley and Sons Inc
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Online AccessGet full text
ISSN1865-1674
1865-1682
1865-1682
DOI10.1111/tbed.14490

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Abstract In 2016–2017, France experienced a devastating epidemic of highly pathogenic avian influenza (HPAI) H5N8, with more than 400 outbreaks reported in poultry farms. We analyzed the spatiotemporal dynamics of the epidemic using a structured‐coalescent‐based phylodynamic approach that combined viral genomic data (n = 196; one viral genome per farm) and epidemiological data. In the process, we estimated viral migration rates between départements (French administrative regions) and the temporal dynamics of the effective viral population size (Ne) in each département. Viral migration rates quantify viral spread between départements and Ne is a population genetic measure of the epidemic size and, in turn, is indicative of the within‐département transmission intensity. We extended the phylodynamic analysis with a generalized linear model to assess the impact of multiple factors—including large‐scale preventive culling and live‐duck movement bans—on viral migration rates and Ne. We showed that the large‐scale culling of ducks that was initiated on 4 January 2017 significantly reduced the viral spread between départements. No relationship was found between the viral spread and duck movements between départements. The within‐département transmission intensity was found to be weakly associated with the intensity of duck movements within départements. Together, these results indicated that the virus spread in short distances, either between adjacent départements or within départements. Results also suggested that the restrictions on duck transport within départements might not have stopped the viral spread completely. Overall, we demonstrated the usefulness of phylodynamics in characterizing the dynamics of a HPAI epidemic and assessing control measures. This method can be adapted to investigate other epidemics of fast‐evolving livestock pathogens.
AbstractList In 2016-2017, France experienced a devastating epidemic of highly pathogenic avian influenza (HPAI) H5N8, with more than 400 outbreaks reported in poultry farms. We analyzed the spatiotemporal dynamics of the epidemic using a structured-coalescent-based phylodynamic approach that combined viral genomic data (n = 196; one viral genome per farm) and epidemiological data. In the process, we estimated viral migration rates between départements (French administrative regions) and the temporal dynamics of the effective viral population size (Ne) in each département. Viral migration rates quantify viral spread between départements and Ne is a population genetic measure of the epidemic size and, in turn, is indicative of the within-département transmission intensity. We extended the phylodynamic analysis with a generalized linear model to assess the impact of multiple factors-including large-scale preventive culling and live-duck movement bans-on viral migration rates and Ne. We showed that the large-scale culling of ducks that was initiated on 4 January 2017 significantly reduced the viral spread between départements. No relationship was found between the viral spread and duck movements between départements. The within-département transmission intensity was found to be weakly associated with the intensity of duck movements within départements. Together, these results indicated that the virus spread in short distances, either between adjacent départements or within départements. Results also suggested that the restrictions on duck transport within départements might not have stopped the viral spread completely. Overall, we demonstrated the usefulness of phylodynamics in characterizing the dynamics of a HPAI epidemic and assessing control measures. This method can be adapted to investigate other epidemics of fast-evolving livestock pathogens.In 2016-2017, France experienced a devastating epidemic of highly pathogenic avian influenza (HPAI) H5N8, with more than 400 outbreaks reported in poultry farms. We analyzed the spatiotemporal dynamics of the epidemic using a structured-coalescent-based phylodynamic approach that combined viral genomic data (n = 196; one viral genome per farm) and epidemiological data. In the process, we estimated viral migration rates between départements (French administrative regions) and the temporal dynamics of the effective viral population size (Ne) in each département. Viral migration rates quantify viral spread between départements and Ne is a population genetic measure of the epidemic size and, in turn, is indicative of the within-département transmission intensity. We extended the phylodynamic analysis with a generalized linear model to assess the impact of multiple factors-including large-scale preventive culling and live-duck movement bans-on viral migration rates and Ne. We showed that the large-scale culling of ducks that was initiated on 4 January 2017 significantly reduced the viral spread between départements. No relationship was found between the viral spread and duck movements between départements. The within-département transmission intensity was found to be weakly associated with the intensity of duck movements within départements. Together, these results indicated that the virus spread in short distances, either between adjacent départements or within départements. Results also suggested that the restrictions on duck transport within départements might not have stopped the viral spread completely. Overall, we demonstrated the usefulness of phylodynamics in characterizing the dynamics of a HPAI epidemic and assessing control measures. This method can be adapted to investigate other epidemics of fast-evolving livestock pathogens.
In 2016–2017, France experienced a devastating epidemic of highly pathogenic avian influenza (HPAI) H5N8, with more than 400 outbreaks reported in poultry farms. We analyzed the spatiotemporal dynamics of the epidemic using a structured‐coalescent‐based phylodynamic approach that combined viral genomic data ( n  = 196; one viral genome per farm) and epidemiological data. In the process, we estimated viral migration rates between départements (French administrative regions) and the temporal dynamics of the effective viral population size ( Ne ) in each département . Viral migration rates quantify viral spread between départements and Ne is a population genetic measure of the epidemic size and, in turn, is indicative of the within‐ département transmission intensity. We extended the phylodynamic analysis with a generalized linear model to assess the impact of multiple factors—including large‐scale preventive culling and live‐duck movement bans—on viral migration rates and Ne . We showed that the large‐scale culling of ducks that was initiated on 4 January 2017 significantly reduced the viral spread between départements . No relationship was found between the viral spread and duck movements between départements . The within‐ département transmission intensity was found to be weakly associated with the intensity of duck movements within départements . Together, these results indicated that the virus spread in short distances, either between adjacent départements or within départements . Results also suggested that the restrictions on duck transport within départements might not have stopped the viral spread completely. Overall, we demonstrated the usefulness of phylodynamics in characterizing the dynamics of a HPAI epidemic and assessing control measures. This method can be adapted to investigate other epidemics of fast‐evolving livestock pathogens.
In 2016–2017, France experienced a devastating epidemic of highly pathogenic avian influenza (HPAI) H5N8, with more than 400 outbreaks reported in poultry farms. We analyzed the spatiotemporal dynamics of the epidemic using a structured‐coalescent‐based phylodynamic approach that combined viral genomic data (n = 196; one viral genome per farm) and epidemiological data. In the process, we estimated viral migration rates between départements (French administrative regions) and the temporal dynamics of the effective viral population size (Ne) in each département. Viral migration rates quantify viral spread between départements and Ne is a population genetic measure of the epidemic size and, in turn, is indicative of the within‐département transmission intensity. We extended the phylodynamic analysis with a generalized linear model to assess the impact of multiple factors—including large‐scale preventive culling and live‐duck movement bans—on viral migration rates and Ne. We showed that the large‐scale culling of ducks that was initiated on 4 January 2017 significantly reduced the viral spread between départements. No relationship was found between the viral spread and duck movements between départements. The within‐département transmission intensity was found to be weakly associated with the intensity of duck movements within départements. Together, these results indicated that the virus spread in short distances, either between adjacent départements or within départements. Results also suggested that the restrictions on duck transport within départements might not have stopped the viral spread completely. Overall, we demonstrated the usefulness of phylodynamics in characterizing the dynamics of a HPAI epidemic and assessing control measures. This method can be adapted to investigate other epidemics of fast‐evolving livestock pathogens.
In 2016-2017, France experienced a devastating epidemic of highly pathogenic avian influenza (HPAI) H5N8, with more than 400 outbreaks reported in poultry farms. We analyzed the spatiotemporal dynamics of the epidemic using a structured-coalescent-based phylodynamic approach that combined viral genomic data (n = 196; one viral genome per farm) and epidemiological data. In the process, we estimated viral migration rates between départements (French administrative regions) and the temporal dynamics of the effective viral population size (Ne) in each département. Viral migration rates quantify viral spread between départements and Ne is a population genetic measure of the epidemic size and, in turn, is indicative of the within-département transmission intensity. We extended the phylodynamic analysis with a generalized linear model to assess the impact of multiple factors-including large-scale preventive culling and live-duck movement bans-on viral migration rates and Ne. We showed that the large-scale culling of ducks that was initiated on 4 January 2017 significantly reduced the viral spread between départements. No relationship was found between the viral spread and duck movements between départements. The within-département transmission intensity was found to be weakly associated with the intensity of duck movements within départements. Together, these results indicated that the virus spread in short distances, either between adjacent départements or within départements. Results also suggested that the restrictions on duck transport within départements might not have stopped the viral spread completely. Overall, we demonstrated the usefulness of phylodynamics in characterizing the dynamics of a HPAI epidemic and assessing control measures. This method can be adapted to investigate other epidemics of fast-evolving livestock pathogens.
Author Chakraborty, Debapriyo
Scoizec, Axelle
Grasland, Beatrice
Briand, Francois‐Xavier
Guinat, Claire
Paul, Mathilde C.
Lebouquin, Sophie
Schmitz, Audrey
Vergne, Timothée
Müller, Nicola F.
Andraud, Mathieu
Niqueux, Eric
Guerin, Jean‐Luc
AuthorAffiliation 5 French Agency for Food, Environmental and Occupational Health & Safety (ANSES) Laboratory of Ploufragan‐Plouzané‐Niort Ploufragan France
2 Department of Biosystems Science and Engineering ETH Zürich Mattenstrasse Basel Switzerland
3 Swiss Institute of Bioinformatics (SIB) Lausanne Switzerland
4 Vaccine and Infectious Disease Fred Hutchinson Cancer Research Centre Seattle Washington USA
1 IHAP Université de Toulouse, INRAE, ENVT Toulouse France
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Issue 5
Keywords outbreak analytics
reconstruction of viral transmission
modelling infectious disease dynamics
emerging infectious diseases
virus evolution
virus molecular epidemiology
Language English
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Snippet In 2016–2017, France experienced a devastating epidemic of highly pathogenic avian influenza (HPAI) H5N8, with more than 400 outbreaks reported in poultry...
In 2016-2017, France experienced a devastating epidemic of highly pathogenic avian influenza (HPAI) H5N8, with more than 400 outbreaks reported in poultry...
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SourceType Open Access Repository
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StartPage e1574
SubjectTerms Animal biology
Animals
Aquatic birds
Avian flu
avian influenza
Culling
Disease control
Disease Outbreaks - veterinary
Ducks
emerging infectious diseases
Epidemics
Epidemiology
Farms
France
France - epidemiology
Generalized linear models
genomics
Influenza
Influenza A Virus, H5N8 Subtype - genetics
Influenza in Birds
Life Sciences
linear models
Livestock
modelling infectious disease dynamics
Original
outbreak analytics
Population genetics
Population number
population size
Poultry
Poultry Diseases
Poultry farming
reconstruction of viral transmission
Statistical models
temporal variation
Veterinary medicine and animal Health
viral genome
virus evolution
virus molecular epidemiology
viruses
Waterfowl
Title Phylodynamic analysis of the highly pathogenic avian influenza H5N8 epidemic in France, 2016–2017
URI https://onlinelibrary.wiley.com/doi/abs/10.1111%2Ftbed.14490
https://www.ncbi.nlm.nih.gov/pubmed/35195353
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https://pubmed.ncbi.nlm.nih.gov/PMC9790735
Volume 69
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