All Title Author
Keywords Abstract

PLOS ONE  2014 

Environmental Correlates of H5N2 Low Pathogenicity Avian Influenza Outbreak Heterogeneity in Domestic Poultry in Italy

DOI: 10.1371/journal.pone.0086788

Full-Text   Cite this paper   Add to My Lib


Italy has experienced recurrent incursions of H5N2 avian influenza (AI) viruses in different geographical areas and varying sectors of the domestic poultry industry. Considering outbreak heterogeneity rather than treating all outbreaks of low pathogenicity AI (LPAI) viruses equally is important given their interactions with the environment and potential to spread, evolve and increase pathogenicity. This study aims at identifying potential environmental drivers of H5N2 LPAI outbreak occurrence in time, space and poultry populations. Thirty-four environmental variables were tested for association with the characteristics of 27 H5N2 LPAI outbreaks (i.e. time, place, flock type, number and species of birds affected) occurred among domestic poultry flocks in Italy in 2010–2012. This was done by applying a recently proposed analytical approach based on a combined non-metric multidimensional scaling, clustering and regression analysis. Results indicated that the pattern of (dis)similarities among the outbreaks entailed an underlying structure that may be the outcome of large-scale, environmental interactions in ecological dimension. Increased densities of poultry breeders, and increased land coverage by industrial, commercial and transport units were associated with increased heterogeneity in outbreak characteristics. In areas with high breeder densities and with many infrastructures, outbreaks affected mainly industrial turkey/layer flocks. Outbreaks affecting ornamental, commercial and rural multi-species flocks occurred mainly in lowly infrastructured areas of northern Italy. Outbreaks affecting rural layer flocks occurred mainly in areas with low breeder densities in south-central Italy. In savannah-like environments, outbreaks affected mainly commercial flocks of galliformes. Suggestive evidence that ecological ordination makes sense genetically was also provided, as virus strains showing high genetic similarity clustered into ecologically similar outbreaks. Findings were informed by hypotheses about how ecological interactions among poultry populations, viruses and their environments can be related to the observed patterns of H5N2 LPAI occurrence. This may prove useful in enhancing future interventions by developing site-specific, ecologically-grounded strategies.


[1]  Alexander DJ (2003) Should we change the definition of avian influenza for eradication purposes? Avian Dis 47: 976–981.
[2]  Sartore S, Bonfanti L, Lorenzetto M, Cecchinato M, Marangon S (2010) The effects of control measures on the economic burden associated with epidemics of avian influenza in Italy. Poult Sci 89: 1115–1121.
[3]  Horimoto T, Kawaoka Y (2001) Pandemic threat posed by avian influenza A viruses. Clin Microbiol Rev 14: 129–149.
[4]  Kawaoka Y, Naeve CW, Webster RG (1984) Is virulence of H5N2 influenza viruses in chickens associated with loss of carbohydrate from the hemagglutinin? Virology 139: 303–316.
[5]  Horimoto T, Rivera E, Pearson J, Senne D, Krauss S, et al. (1995) Origin and molecular changes associated with emergence of a highly pathogenic H5N2 influenza virus in Mexico. Virology 213: 223–230.
[6]  Capua I, Marangon S, Selli L, Alexander DJ, Swayne DE, et al. (1999) Outbreaks of highly pathogenic avian influenza (H5N2) in Italy during October 1997 to January 1998. Avian Pathol 28: 455–460.
[7]  Ogata T, Yamazaki Y, Okabe N, Nakamura Y, Tashiro M, et al. (2008) Human H5N2 avian influenza infection in Japan and the factors associated with high H5N2-neutralizing antibody titer. J Epidemiol 18: 160–166.
[8]  Yamazaki Y, Doy M, Okabe N, Yasui Y, Nakashima K, et al. (2009) Serological survey of avian H5N2-subtype influenza virus infections in human populations. Arch Virol 154: 421–427.
[9]  Mulatti P, Bos MEH, Busani L, Nielen M, Marangon S (2010) Evaluation of interventions and vaccination strategies for low pathogenicity avian influenza: spatial and space-time analyses and quantification of the spread of infection. Epidemiol Infect 138: 813–824.
[10]  Capua I, Marangon S (2007) Control and prevention of avian influenza in an evolving scenario. Vaccine 25: 5645–5652.
[11]  Cecchinato M, Ceolin C, Busani L, Dalla Pozza M, Terregino C, et al. (2010) Low pathogenicity avian influenza in Italy during 2007 and 2008: epidemiology and control. Avian Dis 54: 323–328.
[12]  Martin V, Pfeiffer DU, Zhou X, Xiao X, Prosser DJ, et al. (2011) Spatial distribution and risk factors of highly pathogenic avian influenza (HPAI) H5N1 in China. PLoS Pathog 7: e1001308.
[13]  Gilbert M, Pfeiffer DU (2012) Risk factor modelling of the spatio-temporal patterns of highly pathogenic avian influenza (HPAIV) H5N1: a review. Spat Spatiotemporal Epidemiol 3: 173–183.
[14]  Pfeiffer DU, Minh PQ, Martin V, Epprecht M, Otte MJ (2007) An analysis of the spatial and temporal patterns of highly pathogenic avian influenza occurrence in Vietnam using national surveillance data. Vet J 174: 302–309.
[15]  Carrel MA, Emch M, Nguyen T, Todd Jobe R, Wan X-F (2012) Population-environment drivers of H5N1 avian influenza molecular change in Vietnam. Health Place 18: 1122–1131.
[16]  Mayer JD (2000) Geography, ecology and emerging infectious diseases. Soc Sci Med 50: 937–952.
[17]  Cox TF, Cox MAA (2000) Multidimensional Scaling. London: Chapman and Hall/CRC. 328 p.
[18]  Gower JC (1971) A general coefficient of similarity and some of its properties. Biometrics 27: 857.
[19]  Ward JH (1963) Hierarchical grouping to optimize an objective function. J Am Stat Ass 58: 236.
[20]  Cattoli G, Monne I, Fusaro A, Joannis TM, Lombin LH, et al. (2009) Highly pathogenic avian influenza virus subtype H5N1 in Africa: a comprehensive phylogenetic analysis and molecular characterization of isolates. PLoS ONE 4: e4842.
[21]  Rambaut A (2007) Sequence alignment editor, version 2.0. Available from:
[22]  Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696–704.
[23]  Wilgenbusch JC, Swofford D (2003) Inferring evolutionary trees with PAUP*. Curr Protoc Bioinformatics 6: 6.4.
[24]  Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14: 817–818.
[25]  Nishiguchi A, Kobayashi S, Yamamoto T, Ouchi Y, Sugizaki T, et al. (2007) Risk factors for the introduction of avian influenza virus into commercial layer chicken farms during the outbreaks caused by a low-pathogenic H5N2 virus in Japan in 2005. Zoonoses Public Health 54: 337–343.
[26]  Nishiguchi A, Kobayashi S, Ouchi Y, Yamamoto T, Hayama Y, et al. (2009) Spatial analysis of low pathogenic H5N2 avian influenza outbreaks in Japan in 2005. J Vet Med Sci 71: 979–982.
[27]  Plowright RK, Sokolow SH, Gorman ME, Daszak P, Foley JE (2008) Causal inference in disease ecology: investigating ecological drivers of disease emergence. Front Ecol Environ 6: 420–429.
[28]  Brown JD, Swayne DE, Cooper RJ, Burns RE, Stallknecht DE (2007) Persistence of H5 and H7 avian influenza viruses in water. Avian Dis 51: 285–289.
[29]  Busani L, Valsecchi MG, Rossi E, Toson M, Ferrè N, et al. (2009) Risk factors for highly pathogenic H7N1 avian influenza virus infection in poultry during the 1999–2000 epidemic in Italy. Vet J 181: 171–177.
[30]  Capua I, Marangon S (2000) The avian influenza epidemic in Italy, 1999–2000: a review. Avian Pathol 29: 289–294.
[31]  Boender GJ, Meester R, Gies E, De Jong MCM (2007) The local threshold for geographical spread of infectious diseases between farms. Prev Vet Med 82: 90–101.
[32]  Marangon S, Bortolotti L, Capua I, Bettio M, Dalla Pozza M (2003) Low-pathogenicity avian influenza (LPAI) in Italy (2000–01): epidemiology and control. Avian Dis 47: 1006–1009.
[33]  Cecchinato M, Comin A, Bonfanti L, Terregino C, Monne I, et al. (2011) Epidemiology and control of low pathogenicity avian influenza infections in rural poultry in Italy. Avian Dis 55: 13–20.
[34]  Busani L, Toson M, Stegeman A, Pozza MD, Comin A, et al. (2009) Vaccination reduced the incidence of outbreaks of low pathogenicity avian influenza in northern Italy. Vaccine 27: 3655–3661.


comments powered by Disqus