1887
Research article Open Access
Like 0

Abstract

Introduction

France is one of Europe’s foremost poultry producers and the world’s fifth largest producer of poultry meat. In November 2016, highly pathogenic avian influenza (HPAI) virus subtype H5N8 emerged in poultry in the country. As of 23 March 2017, a total of 484 confirmed outbreaks were reported, with consequences on animal health and socio-economic impacts for producers. We examined the spatio-temporal distribution of outbreaks that occurred in France between November 2016 and March 2017, using the space–time K-function and space–time permutation model of the scan statistic test. : Most outbreaks affected duck flocks in south-west France. A significant space–time interaction of outbreaks was present at the beginning of the epidemic within a window of 8 km and 13 days. This interaction disappeared towards the epidemic end. Five spatio-temporal outbreak clusters were identified in the main poultry producing areas, moving sequentially from east to west. The average spread rate of the epidemic front wave was estimated to be 5.5 km/week. It increased from February 2017 and was negatively associated with the duck holding density. : HPAI-H5N8 infections varied over time and space in France. Intense transmission events occurred at the early stages of the epidemic, followed by long-range jumps in the disease spread towards its end. Findings support strict control strategies in poultry production as well as the maintenance of high biosecurity standards for poultry holdings. Factors and mechanisms driving HPAI spread need to be further investigated.

Loading

Article metrics loading...

/content/10.2807/1560-7917.ES.2018.23.26.1700791
2018-06-28
2024-12-27
/content/10.2807/1560-7917.ES.2018.23.26.1700791
Loading
Loading full text...

Full text loading...

/deliver/fulltext/eurosurveillance/23/26/eurosurv-23-26-1.html?itemId=/content/10.2807/1560-7917.ES.2018.23.26.1700791&mimeType=html&fmt=ahah

References

  1. European Food Safety Authority (EFSA). Avian influenza overview October 2016 - August 2017. EFSA J. 2017;15(10):5018. [Accessed Oct 2017]. Available from: https://www.efsa.europa.eu/en/efsajournal/pub/5018 https://doi.org/10.2903/j.efsa.2017.5018. 
  2. Food and Agriculture Organization of the United Nations (FAO). EMPRES Global Animal Disease Information System (EMPRES-i). Rome: FAO. [Accessed Oct 2017]. Available from: http://empres-i.fao.org/eipws3g/
  3. Food and Agriculture Organization of the United Nations (FAO). Small commercial and family poultry production in France: Characteristics, and impact of HPAI regulations. Rome: FAO; 2010. Available from: http://www.fao.org/docrep/013/al673e/al673e00.pdf
  4. European Food Safety Authority (EFSA). Urgent request on avian influenza. EFSA J. 2017;15(1):4687. [Accessed May 2017]. Available from: https://www.efsa.europa.eu/fr/efsajournal/pub/4687 https://doi.org/10.2903/j.efsa.2016.4687. 
  5. Le Bouquin S, Huneau-Salaun A, Hamon M, Moisson MC, Scoizec A, Niqueux E, et al. L’épisode d’influenza aviaire en France en 2015-2016 - Situation épidémiologique au 30 juin 2016. Bulletin épidémiologique, santé animale et alimentation. 2016;75. French. [Accessed in Oct 2017]. Available from: http://bulletinepidemiologique.mag.anses.fr/sites/default/files/2017-03-01_maquette%20BE_surveillance%20IA_0.pdf
  6. Núñez A, Brookes SM, Reid SM, Garcia-Rueda C, Hicks DJ, Seekings JM, et al. Highly Pathogenic Avian Influenza H5N8 Clade 2.3.4.4 Virus: Equivocal Pathogenicity and Implications for Surveillance Following Natural Infection in Breeder Ducks in the United Kingdom. Transbound Emerg Dis. 2016;63(1):5-9.  https://doi.org/10.1111/tbed.12442  PMID: 26519234 
  7. Briand F-X, Schmitz A, Ogor K, Le Prioux A, Guillou-Cloarec C, Guillemoto C, et al. Emerging highly pathogenic H5 avian influenza viruses in France during winter 2015/16: phylogenetic analyses and markers for zoonotic potential. Euro Surveill. 2017;22(9):30473.  https://doi.org/10.2807/1560-7917.ES.2017.22.9.30473  PMID: 28277218 
  8. Institut national de l'information géographique et forestière (IGN). GEOFLA. IGN. Available from: http://professionnels.ign.fr/geofla
  9. R Development Core Team. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2011. ISBN 3-900051-07-0. [Accessed in April 2017]. Available from: http://www.R-project.org
  10. French Agency for Food. Environmental and Occupational Health & Safety (ANSES). AVIS de l’Agence nationale de sécurité sanitaire de l’alimentation, de l’environnement et du travail relatif au « périmètre optimal de dépeuplement préventif influenza aviaire IA HP H5N8 ». Maisons-Alfort: ANSES; 2017. French. [Accessed Apr 2017]. Available from: https://www.anses.fr/fr/system/files/SABA2017SA0011.pdf
  11. Diggle PJ, Chetwynd AG, Häggkvist R, Morris SE. Second-order analysis of space-time clustering. Stat Methods Med Res. 1995;4(2):124-36.  https://doi.org/10.1177/096228029500400203  PMID: 7582201 
  12. Vergne T, Gogin A, Pfeiffer DU. Statistical Exploration of Local Transmission Routes for African Swine Fever in Pigs in the Russian Federation, 2007-2014. Transbound Emerg Dis. 2017;64(2):504-12.  https://doi.org/10.1111/tbed.12391  PMID: 26192820 
  13. Métras R, Porphyre T, Pfeiffer DU, Kemp A, Thompson PN, Collins LM, et al. Exploratory space-time analyses of Rift Valley Fever in South Africa in 2008-2011. PLoS Negl Trop Dis. 2012;6(8):e1808.  https://doi.org/10.1371/journal.pntd.0001808  PMID: 22953020 
  14. Rowlingson BS, Diggle PJ. Splancs: Spatial point pattern analysis code in S-plus. Comput Geosci. 1993;19(5):627-55.  https://doi.org/10.1016/0098-3004(93)90099-Q 
  15. Kulldorff M, Huang L, Konty K. A scan statistic for continuous data based on the normal probability model. Int J Health Geogr. 2009;8(1):58.  https://doi.org/10.1186/1476-072X-8-58  PMID: 19843331 
  16. Porphyre T, McKenzie J, Stevenson M. A descriptive spatial analysis of bovine tuberculosis in intensively controlled cattle farms in New Zealand. Vet Res. 2007;38(3):465-79.  https://doi.org/10.1051/vetres:2007003  PMID: 17425934 
  17. Picado A, Speybroeck N, Kivaria F, Mosha RM, Sumaye RD, Casal J, et al. Foot-and-mouth disease in Tanzania from 2001 to 2006. Transbound Emerg Dis. 2011;58(1):44-52.  https://doi.org/10.1111/j.1865-1682.2010.01180.x  PMID: 21078082 
  18. Kulldorff. Information Management Services Inc. SatScan v9.4: Software for the spatial and space-time scan statistics. [Accessed in April 2017]. Available from: http://www.satscan.org
  19. Tisseuil C, Gryspeirt A, Lancelot R, Pioz M, Liebhold A, Gilbert M. Evaluating methods to quantify spatial variation in the velocity of biological invasions. Ecography. 2016;39(5):409-18.  https://doi.org/10.1111/ecog.01393 
  20. Nicolas G, Tisseuil C, Conte A, Allepuz A, Pioz M, Lancelot R, et al. Environmental heterogeneity and variations in the velocity of bluetongue virus spread in six European epidemics. Prev Vet Med. 2018;149:1-9.  https://doi.org/10.1016/j.prevetmed.2017.11.005  PMID: 29290289 
  21. Nychka D, Furrer R, Paige J, Sain S. Package ‘fields’. [Accessed in April 2017]. Available from: https://cran.r-project.org/web/packages/fields/fields.pdf
  22. Boender GJ, Hagenaars TJ, Bouma A, Nodelijk G, Elbers AR, de Jong MC, et al. Risk maps for the spread of highly pathogenic avian influenza in poultry. PLOS Comput Biol. 2007;3(4):e71.  https://doi.org/10.1371/journal.pcbi.0030071  PMID: 17447838 
  23. Ypma RJF, Jonges M, Bataille A, Stegeman A, Koch G, van Boven M, et al. Genetic data provide evidence for wind-mediated transmission of highly pathogenic avian influenza. J Infect Dis. 2013;207(5):730-5.  https://doi.org/10.1093/infdis/jis757  PMID: 23230058 
  24. Ssematimba A, Hagenaars TJ, de Jong MCM. Modelling the wind-borne spread of highly pathogenic avian influenza virus between farms. PLoS One. 2012;7(2):e31114.  https://doi.org/10.1371/journal.pone.0031114  PMID: 22348042 
  25. Thulke H-H, Eisinger D, Beer M. The role of movement restrictions and pre-emptive destruction in the emergency control strategy against CSF outbreaks in domestic pigs. Prev Vet Med. 2011;99(1):28-37.  https://doi.org/10.1016/j.prevetmed.2011.01.002  PMID: 21300412 
  26. Tildesley MJ, Bessell PR, Keeling MJ, Woolhouse ME. The role of pre-emptive culling in the control of foot-and-mouth disease. Proc Biol Sci. 2009;276(1671):3239-48.  https://doi.org/10.1098/rspb.2009.0427  PMID: 19570791 
  27. Jourdain E, Gauthier-Clerc M, Bicout DJ, Sabatier P. Bird migration routes and risk for pathogen dispersion into western Mediterranean wetlands. Emerg Infect Dis. 2007;13(3):365-72.  https://doi.org/10.3201/eid1303.060301  PMID: 17552088 
  28. Gaidet N, Cappelle J, Takekawa JY, Prosser DJ, Iverson SA, Douglas DC, et al. Potential spread of highly pathogenic avian influenza H5N1 by wildfowl: dispersal ranges and rates determined from large-scale satellite telemetry. J Appl Ecol. 2010;47(5):1147-57.  https://doi.org/10.1111/j.1365-2664.2010.01845.x 
  29. French Agency for Food. Environmental and Occupational Health & Safety (ANSES). Plateforme Epidémiosurveillance Santé Animale, Situation de l’influenza aviaire en France au 18/04/2017; 2017. [Accessed Apr 2017]. Available from: http://plateforme-esa.fr/article/situation-de-l-influenza-aviaire-en-france-au-18042017-20h00
  30. Pantin-Jackwood MJ, Costa-Hurtado M, Shepherd E, DeJesus E, Smith D, Spackman E, et al. Pathogenicity and Transmission of H5 and H7 Highly Pathogenic Avian Influenza Viruses in Mallards. J Virol. 2016;90(21):9967-82.  https://doi.org/10.1128/JVI.01165-16  PMID: 27558429 
/content/10.2807/1560-7917.ES.2018.23.26.1700791
Loading

Data & Media loading...

Supplementary data

Submit comment
Close
Comment moderation successfully completed
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error