Influenza A H5N1 and H7N9 in China: A spatial risk analysis

Background Zoonotic avian influenza poses a major risk to China, and other parts of the world. H5N1 has remained endemic in China and globally for nearly two decades, and in 2013, a novel zoonotic influenza A subtype H7N9 emerged in China. This study aimed to improve upon our current understanding of the spreading mechanisms of H7N9 and H5N1 by generating spatial risk profiles for each of the two virus subtypes across mainland China. Methods and findings In this study, we (i) developed a refined data set of H5N1 and H7N9 locations with consideration of animal/animal environment case data, as well as spatial accuracy and precision; (ii) used this data set along with environmental variables to build species distribution models (SDMs) for each virus subtype in high resolution spatial units of 1km2 cells using Maxent; (iii) developed a risk modelling framework which integrated the results from the SDMs with human and chicken population variables, which was done to quantify the risk of zoonotic transmission; and (iv) identified areas at high risk of H5N1 and H7N9 transmission. We produced high performing SDMs (6 of 8 models with AUC > 0.9) for both H5N1 and H7N9. In all our SDMs, H7N9 consistently showed higher AUC results compared to H5N1, suggesting H7N9 suitability could be better explained by environmental variables. For both subtypes, high risk areas were primarily located in south-eastern China, with H5N1 distributions found to be more diffuse and extending more inland compared to H7N9. Conclusions We provide projections of our risk models to public health policy makers so that specific high risk areas can be targeted for control measures. We recommend comparing H5N1 and H7N9 prevalence rates and survivability in the natural environment to better understand the role of animal and environmental transmission in human infections.

[1]  D. Suarez,et al.  Role of Poultry in the Spread of Novel H7N9 Influenza Virus in China , 2014, Journal of Virology.

[2]  Chuanhua Yu,et al.  Spatiotemporal pattern and risk factors of the reported novel avian-origin influenza A(H7N9) cases in China. , 2014, Preventive veterinary medicine.

[3]  Huidong Tian,et al.  Global Occurrence and Spread of Highly Pathogenic Avian Influenza Virus of the Subtype H5N1 , 2011, Avian diseases.

[4]  Maia Martcheva,et al.  MODELING SEASONALITY IN AVIAN INFLUENZA H5N1 , 2013 .

[5]  Zhen Jin,et al.  Pattern transitions in spatial epidemics: Mechanisms and emergent properties , 2016, Physics of Life Reviews.

[6]  Ke Bingsheng,et al.  Poultry sector in China : structural changes during the past decade and future trends , 2008 .

[7]  S. Hay,et al.  Mapping the Global Distribution of Livestock , 2014, PloS one.

[8]  S. Sarkar,et al.  A Predictive Spatial Model to Quantify the Risk of Air-Travel-Associated Dengue Importation into the United States and Europe , 2012, Journal of tropical medicine.

[9]  D. Pfeiffer,et al.  Can closure of live poultry markets halt the spread of H7N9? , 2014, The Lancet.

[10]  Miroslav Dudík,et al.  Modeling of species distributions with Maxent: new extensions and a comprehensive evaluation , 2008 .

[11]  R. Pearson,et al.  Predicting species distributions from small numbers of occurrence records: A test case using cryptic geckos in Madagascar , 2006 .

[12]  A. Chughtai,et al.  Quantified degree of poultry exposure differs for human cases of avian influenza H5N1 and H7N9 , 2016, Epidemiology and Infection.

[13]  Wu-Chun Cao,et al.  Mapping Spread and Risk of Avian Influenza A (H7N9) in China , 2013, Scientific Reports.

[14]  Wu-Chun Cao,et al.  Risk Distribution of Human Infections with Avian Influenza H7N9 and H5N1 virus in China , 2015, Scientific Reports.

[15]  Matthew J. Smith,et al.  Protected areas network is not adequate to protect a critically endangered East Africa Chelonian: Modelling distribution of pancake tortoise, Malacochersus tornieri under current and future climates , 2013, bioRxiv.

[16]  M. Gilbert,et al.  Characterizing the interface between wild ducks and poultry to evaluate the potential of transmission of avian pathogens , 2011, International journal of health geographics.

[17]  Yuqi Bai,et al.  Climate change suggests a shift of H5N1 risk in migratory birds , 2015 .

[18]  M. Gilbert,et al.  Avian influenza, domestic ducks and rice agriculture in Thailand. , 2007, Agriculture, ecosystems & environment.

[19]  Xianning Liu,et al.  Avian-human influenza epidemic model. , 2007, Mathematical biosciences.

[20]  Nick Golding,et al.  Fast and flexible Bayesian species distribution modelling using Gaussian processes , 2016 .

[21]  M. Gilbert,et al.  Modeling habitat suitability for occurrence of highly pathogenic avian influenza virus H5N1 in domestic poultry in Asia: a spatial multicriteria decision analysis approach. , 2013, Spatial and spatio-temporal epidemiology.

[22]  A. Peterson,et al.  Ecology and geography of avian influenza (HPAI H5N1) transmission in the Middle East and northeastern Africa , 2009, International journal of health geographics.

[23]  Trevor Hastie,et al.  A statistical explanation of MaxEnt for ecologists , 2011 .

[24]  A. A. Hill,et al.  Modelling the species jump: towards assessing the risk of human infection from novel avian influenzas , 2015, Royal Society Open Science.

[25]  A. Peterson,et al.  Comparative analysis of remotely-sensed data products via ecological niche modeling of avian influenza case occurrences in Middle Eastern poultry , 2011, International journal of health geographics.

[26]  J. Brashares,et al.  The effects of small sample size and sample bias on threshold selection and accuracy assessment of species distribution models , 2012 .

[27]  Yuqi Bai,et al.  Inference and forecast of H7N9 influenza in China, 2013 to 2015 , 2017, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[28]  M. Klaassen,et al.  Avian influenza infection dynamics under variable climatic conditions, viral prevalence is rainfall driven in waterfowl from temperate, south-east Australia , 2016, Veterinary Research.

[29]  Peter M Atkinson,et al.  Interpreting predictive maps of disease: highlighting the pitfalls of distribution models in epidemiology. , 2014, Geospatial health.

[30]  A. Chughtai,et al.  A Systematic Review of the Comparative Epidemiology of Avian and Human Influenza A H5N1 and H7N9 - Lessons and Unanswered Questions. , 2016, Transboundary and emerging diseases.

[31]  Chi-Tai Fang,et al.  A modeling study of human infections with avian influenza A H7N9 virus in mainland China. , 2015, International journal of infectious diseases : IJID : official publication of the International Society for Infectious Diseases.

[32]  S. Moriguchi,et al.  Potential risk map for avian influenza A virus invading Japan , 2013 .

[33]  C. Cao,et al.  Ecological Niche Modeling of Risk Factors for H7N9 Human Infection in China , 2016, International journal of environmental research and public health.

[34]  Rui Xia,et al.  Effects of closing and reopening live poultry markets on the epidemic of human infection with avian influenza A virus , 2015, Journal of biomedical research.

[35]  S. Dowell,et al.  Seasonality of infectious diseases and severe acute respiratory syndrome–what we don't know can hurt us , 2004, The Lancet Infectious Diseases.

[36]  A. Peterson,et al.  Predictable ecology and geography of avian influenza (H5N1) transmission in Nigeria and West Africa. , 2008, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[37]  Yi Guan,et al.  Dissemination, divergence and establishment of H7N9 influenza viruses in China , 2015, Nature.

[38]  John Steel,et al.  Roles of Humidity and Temperature in Shaping Influenza Seasonality , 2014, Journal of Virology.

[39]  Dirk U. Pfeiffer,et al.  Spatial modelling of disease using data- and knowledge-driven approaches. , 2011, Spatial and spatio-temporal epidemiology.

[40]  M. Jeggo,et al.  Avian Influenza from an Ecohealth Perspective , 2014, EcoHealth.

[41]  X. Su,et al.  Interpreting the transmissibility of the avian influenza A(H7N9) infection from 2013 to 2015 in Zhejiang Province, China , 2015, Epidemiology and Infection.

[42]  David M. Frank,et al.  Chagas Disease Risk in Texas , 2010, PLoS neglected tropical diseases.

[43]  Hongyue WANG,et al.  Log-transformation and its implications for data analysis , 2014, Shanghai archives of psychiatry.

[44]  M. Gilbert,et al.  Risk factor modelling of the spatio-temporal patterns of highly pathogenic avian influenza (HPAIV) H5N1: a review. , 2012, Spatial and spatio-temporal epidemiology.

[45]  A. Peterson,et al.  Continent-wide association of H5N1 outbreaks in wild and domestic birds in Europe. , 2011, Geospatial health.

[46]  R. Gao,et al.  Inactivation of the novel avian influenza A (H7N9) virus under physical conditions or chemical agents treatment , 2013, Virology Journal.

[47]  M. Craft,et al.  Advances and Limitations of Disease Biogeography Using Ecological Niche Modeling , 2016, Front. Microbiol..

[48]  Y. Rao,et al.  Identification of climate factors related to human infection with avian influenza A H7N9 and H5N1 viruses in China , 2015, Scientific Reports.

[49]  L. Fang,et al.  Environmental Factors Contributing to the Spread of H5N1 Avian Influenza in Mainland China , 2008, PloS one.

[50]  Benjamin J Cowling,et al.  Effect of closure of live poultry markets on poultry-to-person transmission of avian influenza A H7N9 virus: an ecological study , 2014, The Lancet.

[51]  Ying-Hen Hsieh,et al.  Quantification of Bird-to-Bird and Bird-to-Human Infections during 2013 Novel H7N9 Avian Influenza Outbreak in China , 2014, PloS one.

[52]  D. Pfeiffer,et al.  Live Poultry Trade in Southern China Provinces and HPAIV H5N1 Infection in Humans and Poultry: The Role of Chinese New Year Festivities , 2012, PloS one.

[53]  M. Gilbert,et al.  Spatial Distribution and Risk Factors of Highly Pathogenic Avian Influenza (HPAI) H5N1 in China , 2011, PLoS pathogens.

[54]  M. Fortin,et al.  Spatial Analysis: A Guide for Ecologists 1st edition , 2005 .

[55]  Catherine Linard,et al.  Predicting the risk of avian influenza A H7N9 infection in live-poultry markets across Asia , 2014, Nature Communications.

[56]  M. Martcheva,et al.  MODELING SEASONALITY IN AVIAN INFLUENZA H 5 N 1 , 2013 .

[57]  H. Mao,et al.  Surveillance of Avian H7N9 Virus in Various Environments of Zhejiang Province, China before and after Live Poultry Markets Were Closed in 2013–2014 , 2015, PloS one.

[58]  A. Peterson,et al.  Effects of sample size on the performance of species distribution models , 2008 .

[59]  Kerrie Mengersen,et al.  Weather variability and influenza A (H7N9) transmission in Shanghai, China: a Bayesian spatial analysis. , 2014, Environmental research.

[60]  T. Bailey Spatial Analysis: A Guide for Ecologists , 2006 .

[61]  Alberto Jiménez-Valverde,et al.  Delimiting the geographical background in species distribution modelling , 2012 .

[62]  E. Lau,et al.  Effect of Live Poultry Market Closure on Avian Influenza A(H7N9) Virus Activity in Guangzhou, China, 2014 , 2015, Emerging infectious diseases.

[63]  Steven J. Phillips Transferability, sample selection bias and background data in presence‐only modelling: a response to Peterson et al. (2007) , 2008 .

[64]  A. Peterson,et al.  Potential Geographic Distribution of the Novel Avian-Origin Influenza A (H7N9) Virus , 2014, PloS one.

[65]  C. Macintyre,et al.  A Meta‐Analysis of the Prevalence of Influenza A H5N1 and H7N9 Infection in Birds , 2017, Transboundary and emerging diseases.

[66]  Li Li,et al.  Patch invasion in a spatial epidemic model , 2015, Appl. Math. Comput..

[67]  Keiko A. Herrick,et al.  A global model of avian influenza prediction in wild birds: the importance of northern regions , 2013, Veterinary Research.

[68]  Ricardo J Soares Magalhães,et al.  Risk-based surveillance for avian influenza control along poultry market chains in South China: The value of social network analysis , 2011, Preventive Veterinary Medicine.

[69]  A. Skidmore,et al.  Environmental factors influencing the spread of the highly pathogenic avian influenza H5N1 virus in wild birds in Europe , 2010 .

[70]  Heinz Mehlhorn,et al.  World Organisation for Animal Health (OIE) , 2015 .

[71]  Ping Zhang,et al.  Modelling the Risk of Highly Pathogenic Avian Influenza H5N1 in Wild Birds and Poultry of China , 2015, GRMSE.

[72]  M. Gilbert,et al.  Mapping H5N1 highly pathogenic avian influenza risk in Southeast Asia , 2008, Proceedings of the National Academy of Sciences.

[73]  P. Kaye Infectious diseases of humans: Dynamics and control , 1993 .

[74]  L. Fang,et al.  Identifying areas with a high risk of human infection with the avian influenza A (H7N9) virus in East Asia. , 2014, The Journal of infection.

[75]  Y. Guan,et al.  Interventions to reduce zoonotic and pandemic risks from avian influenza in Asia. , 2016, The Lancet. Infectious diseases.

[76]  Zhongjie Li,et al.  Poultry Market Closures and Human Infection with Influenza A(H7N9) Virus, China, 2013–14 , 2014, Emerging infectious diseases.

[77]  K. Shortridge Avian influenza A viruses of southern China and Hong Kong: ecological aspects and implications for man. , 1982, Bulletin of the World Health Organization.

[78]  Zhang-yue Zhou,et al.  Food Consumption in China: The Revolution Continues , 2014 .

[79]  D. P. Hayes Influenza pandemics, solar activity cycles, and vitamin D. , 2010, Medical hypotheses.

[80]  Jian Li,et al.  Live Poultry Market Closure and Control of Avian Influenza A(H7N9), Shanghai, China , 2014, Emerging infectious diseases.

[81]  A. Tran,et al.  Quantitative assessment of a spatial multicriteria model for highly pathogenic avian influenza H5N1 in Thailand, and application in Cambodia , 2016, Scientific Reports.

[82]  C. Feng,et al.  The impact of temperature and humidity measures on influenza A (H7N9) outbreaks-evidence from China. , 2015, International journal of infectious diseases : IJID : official publication of the International Society for Infectious Diseases.

[83]  John Bell,et al.  A review of methods for the assessment of prediction errors in conservation presence/absence models , 1997, Environmental Conservation.

[84]  James H. Spencer,et al.  Evidence for the Convergence Model: The Emergence of Highly Pathogenic Avian Influenza (H5N1) in Viet Nam , 2015, PloS one.

[85]  G. Gao,et al.  Newly Emergent Highly Pathogenic H5N9 Subtype Avian Influenza A Virus , 2015, Journal of Virology.

[86]  S. Sarkar,et al.  Malaria in Africa: Vector Species' Niche Models and Relative Risk Maps , 2007, PloS one.