Global mapping of highly pathogenic avian influenza H5N1 and H5Nx clade 2.3.4.4 viruses with spatial cross-validation

  1. Madhur S Dhingra
  2. Jean Artois
  3. Timothy P Robinson
  4. Catherine Linard
  5. Celia Chaiban
  6. Ioannis Xenarios
  7. Robin Engler
  8. Robin Liechti
  9. Dimitry Kuznetsov
  10. Xiangming Xiao
  11. Sophie Von Dobschuetz
  12. Filip Claes
  13. Scott H Newman  Is a corresponding author
  14. Gwenaëlle Dauphin  Is a corresponding author
  15. Marius Gilbert  Is a corresponding author
  1. Université Libre de Bruxelles, Belgium
  2. International Livestock Research Institute, Kenya
  3. Swiss Institute of Bioinformatics, Switzerland
  4. University of Oklahoma, United States
  5. Food and Agriculture Organization of the United Nations, Italy
  6. Regional Office for Asia and the Pacific, Thailand
  7. Food and Agriculture Organization of the United Nations, Vietnam

Abstract

Global disease suitability models are essential tools to inform surveillance systems and enable early detection. We present the first global suitability model of highly pathogenic avian influenza (HPAI) H5N1 and demonstrate that reliable predictions can be obtained at global scale. Best predictions are obtained using spatial predictor variables describing host distributions, rather than land use or eco-climatic spatial predictor variables, with a strong association with domestic duck and extensively raised chicken densities. Our results also support a more systematic use of spatial cross-validation in large-scale disease suitability modelling compared to standard random cross-validation that can lead to unreliable measure of extrapolation accuracy. A global suitability model of the H5 clade 2.3.4.4 viruses, a group of viruses that recently spread extensively in Asia and the US, shows in comparison a lower spatial extrapolation capacity than the HPAI H5N1 models, with a stronger association with intensively raised chicken densities and anthropogenic factors.

Data availability

The following previously published data sets were used

Article and author information

Author details

  1. Madhur S Dhingra

    Spatial Epidemiology Lab, Université Libre de Bruxelles, Brussels, Belgium
    Competing interests
    The authors declare that no competing interests exist.
  2. Jean Artois

    Spatial Epidemiology Lab, Université Libre de Bruxelles, Brussels, Belgium
    Competing interests
    The authors declare that no competing interests exist.
  3. Timothy P Robinson

    Livestock Systems and Environment, International Livestock Research Institute, Nairobi, Kenya
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4266-963X
  4. Catherine Linard

    Spatial Epidemiology Lab, Université Libre de Bruxelles, Brussels, Belgium
    Competing interests
    The authors declare that no competing interests exist.
  5. Celia Chaiban

    Spatial Epidemiology Lab, Université Libre de Bruxelles, Brussels, Belgium
    Competing interests
    The authors declare that no competing interests exist.
  6. Ioannis Xenarios

    Swiss-Prot & Vital-IT group, Swiss Institute of Bioinformatics, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  7. Robin Engler

    Swiss-Prot & Vital-IT group, Swiss Institute of Bioinformatics, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  8. Robin Liechti

    Swiss-Prot & Vital-IT group, Swiss Institute of Bioinformatics, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  9. Dimitry Kuznetsov

    Swiss-Prot & Vital-IT group, Swiss Institute of Bioinformatics, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  10. Xiangming Xiao

    Department of Microbiology and Plant Biology, University of Oklahoma, Norman, United States
    Competing interests
    The authors declare that no competing interests exist.
  11. Sophie Von Dobschuetz

    Animal Production and Health Division, Food and Agriculture Organization of the United Nations, Rome, Italy
    Competing interests
    The authors declare that no competing interests exist.
  12. Filip Claes

    Emergency Center for Transboundary Animal Diseases, Regional Office for Asia and the Pacific, Bangkok, Thailand
    Competing interests
    The authors declare that no competing interests exist.
  13. Scott H Newman

    Emergency Center for Transboundary Animal Diseases, Food and Agriculture Organization of the United Nations, Hanoi, Vietnam
    For correspondence
    scott.newman@fao.org
    Competing interests
    The authors declare that no competing interests exist.
  14. Gwenaëlle Dauphin

    Animal Production and Health Division, Food and Agriculture Organization of the United Nations, Rome, Italy
    For correspondence
    Gwenaelle.Dauphin@fao.org
    Competing interests
    The authors declare that no competing interests exist.
  15. Marius Gilbert

    Spatial Epidemiology Lab, Université Libre de Bruxelles, Brussels, Belgium
    For correspondence
    marius.gilbert@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3708-3359

Funding

National Institutes of Health (1R01AI101028-02A1)

  • Madhur S Dhingra
  • Jean Artois
  • Xiangming Xiao
  • Marius Gilbert

United States Agency for International Development (Emerging Pandemic Threats program)

  • Scott H Newman

Biotechnology and Biological Sciences Research Council (BB/L019019/1)

  • Timothy P Robinson

Fonds De La Recherche Scientifique - FNRS (PDR T.0073.13)

  • Catherine Linard
  • Marius Gilbert

Medical Research Council (ESEI UrbanZoo (G1100783/1))

  • Timothy P Robinson

CGIAR (Research Programs on Agriculture for Nutrition and Health (A4NH) and Livestock)

  • Timothy P Robinson

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

© 2016, Dhingra et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 4,432
    views
  • 777
    downloads
  • 44
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Madhur S Dhingra
  2. Jean Artois
  3. Timothy P Robinson
  4. Catherine Linard
  5. Celia Chaiban
  6. Ioannis Xenarios
  7. Robin Engler
  8. Robin Liechti
  9. Dimitry Kuznetsov
  10. Xiangming Xiao
  11. Sophie Von Dobschuetz
  12. Filip Claes
  13. Scott H Newman
  14. Gwenaëlle Dauphin
  15. Marius Gilbert
(2016)
Global mapping of highly pathogenic avian influenza H5N1 and H5Nx clade 2.3.4.4 viruses with spatial cross-validation
eLife 5:e19571.
https://doi.org/10.7554/eLife.19571

Share this article

https://doi.org/10.7554/eLife.19571

Further reading

    1. Epidemiology and Global Health
    Xiaoning Wang, Jinxiang Zhao ... Dong Liu
    Research Article

    Artificially sweetened beverages containing noncaloric monosaccharides were suggested as healthier alternatives to sugar-sweetened beverages. Nevertheless, the potential detrimental effects of these noncaloric monosaccharides on blood vessel function remain inadequately understood. We have established a zebrafish model that exhibits significant excessive angiogenesis induced by high glucose, resembling the hyperangiogenic characteristics observed in proliferative diabetic retinopathy (PDR). Utilizing this model, we observed that glucose and noncaloric monosaccharides could induce excessive formation of blood vessels, especially intersegmental vessels (ISVs). The excessively branched vessels were observed to be formed by ectopic activation of quiescent endothelial cells (ECs) into tip cells. Single-cell transcriptomic sequencing analysis of the ECs in the embryos exposed to high glucose revealed an augmented ratio of capillary ECs, proliferating ECs, and a series of upregulated proangiogenic genes. Further analysis and experiments validated that reduced foxo1a mediated the excessive angiogenesis induced by monosaccharides via upregulating the expression of marcksl1a. This study has provided new evidence showing the negative effects of noncaloric monosaccharides on the vascular system and the underlying mechanisms.

    1. Epidemiology and Global Health
    2. Microbiology and Infectious Disease
    Amanda C Perofsky, John Huddleston ... Cécile Viboud
    Research Article

    Influenza viruses continually evolve new antigenic variants, through mutations in epitopes of their major surface proteins, hemagglutinin (HA) and neuraminidase (NA). Antigenic drift potentiates the reinfection of previously infected individuals, but the contribution of this process to variability in annual epidemics is not well understood. Here, we link influenza A(H3N2) virus evolution to regional epidemic dynamics in the United States during 1997—2019. We integrate phenotypic measures of HA antigenic drift and sequence-based measures of HA and NA fitness to infer antigenic and genetic distances between viruses circulating in successive seasons. We estimate the magnitude, severity, timing, transmission rate, age-specific patterns, and subtype dominance of each regional outbreak and find that genetic distance based on broad sets of epitope sites is the strongest evolutionary predictor of A(H3N2) virus epidemiology. Increased HA and NA epitope distance between seasons correlates with larger, more intense epidemics, higher transmission, greater A(H3N2) subtype dominance, and a greater proportion of cases in adults relative to children, consistent with increased population susceptibility. Based on random forest models, A(H1N1) incidence impacts A(H3N2) epidemics to a greater extent than viral evolution, suggesting that subtype interference is a major driver of influenza A virus infection ynamics, presumably via heterosubtypic cross-immunity.