Highly Pathogenic Avian Influenza (H5N1)
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viruses Article Highly Pathogenic Avian Influenza (H5N1) Landscape Suitability Varies by Wetland Habitats and the Degree of Interface between Wild Waterfowl and Poultry in India Michael G. Walsh 1,2,3,*, Siobhan M. Mor 4,5 and Shah Hossain 2 1 Faculty of Medicine and Health, Marie Bashir Institute for Infectious Diseases and Biosecurity, The University of Sydney, Westmead, NSW 2145, Australia 2 Faculty of Medicine and Health, School of Public Health, The University of Sydney, Camperdown, NSW 2006, Australia; [email protected] 3 The Prasanna School of Public Health, Manipal Academy of Higher Education, Manipal 576104, Karnataka, India 4 Faculty of Health and Life Sciences, Institute of Infection and Global Health Liverpool, The University of Liverpool, Merseyside L69 3BX, UK; [email protected] 5 International Livestock Research Institute, Addis Ababa 2R87, Ethiopia * Correspondence: [email protected] or [email protected] Received: 24 September 2020; Accepted: 10 November 2020; Published: 11 November 2020 Abstract: Highly pathogenic avian influenza (HPAI) virus, subtype H5N1, constitutes one of the world’s most important health and economic concerns given the catastrophic impact of epizootics on the poultry industry, the high mortality attending spillover in humans, and its potential as a source subtype for a future pandemic. Nevertheless, we still lack an adequate understanding of HPAI H5N1 epidemiology and infection ecology. The nature of the wild waterfowl–poultry interface, and the sharing of diverse wetland habitat among these birds, currently underscore important knowledge gaps. India has emerged as a global hotspot for HPAI H5N1, while also providing critical wintering habitat for many species of migratory waterfowl and year-round habitat for several resident waterfowl species. The current study sought to examine the extent to which the wild waterfowl–poultry interface, varied wetland habitat, and climate influence HPAI H5N1 epizootics in poultry in India. Using World Organisation for Animal Health reported outbreaks, this study showed that the wild waterfowl–poultry interface and lacustrine, riparian, and coastal marsh wetland systems were strongly associated with landscape suitability, and these relationships varied by scale. Although increasing poultry density was associated with increasing risk, this was only the case in the absence of wild waterfowl habitat, and only at a local scale. In landscapes increasingly shared between wild waterfowl and poultry, suitability was greater among lower density poultry, again at a local scale only. These findings provide further insight into the occurrence of HPAI H5N1 in India and suggest important landscape targets for blocking the waterfowl–poultry interface to interrupt virus transmission and prevent future outbreaks. Keywords: avian influenza; H5N1; waterfowl; poultry; waterfowl-poultry interface; wetlands; One Health 1. Introduction Highly pathogenic avian influenza (HPAI) virus, subtype H5N1, presents one of the biggest threats to the agricultural economy and human health. The economic burden associated with outbreaks in poultry is quick and catastrophic due to both the mortality experienced by infected birds and Viruses 2020, 12, 1290; doi:10.3390/v12111290 www.mdpi.com/journal/viruses Viruses 2020, 12, x FOR PEER REVIEW 2 of 14 Viruses 2020, 12, 1290 2 of 14 outbreaks in poultry is quick and catastrophic due to both the mortality experienced by infected birds and the standard practice of culling to prevent further spread [1–3]. The threat to human health is thealso standard substantial practice given of the culling high tofatality prevent associated further spreadwith spillover, [1–3]. Thewhich threat is approximately to human health 60% isfor also substantialHPAI H5N1 given [4]. the Furthermore, high fatality through associated the with ongoing spillover, processes which of is approximatelyinfluenza A mutation 60% for and HPAI H5N1reassortment [4]. Furthermore, and ever-present through theevolutionary ongoing processespressure toward of influenza novel A subtypes, mutation HPAI and reassortmentH5N1 poses anda ever-presentsignificant risk evolutionary as a progenitor pressure for a toward future pandemic novel subtypes, subtype. HPAI H5N1 poses a significant risk as a progenitorThe forglobal a future significance pandemic of subtype. HPAI H5N1 notwithstanding, the infection ecology of viral transmissionThe global significanceremains poorly of HPAI understood, H5N1 notwithstanding, which confounds the optimal infection preventi ecologyon of strategies. viral transmission Wild remainswaterfowl, poorly primarily understood, Anatidae, which are confounds natural reservoirs optimal prevention of avian influenza strategies. A viruses, Wild waterfowl, including primarily HPAI Anatidae,H5 subtypes are natural[1,5]. Migratory reservoirs and ofresidential avian influenza wild waterfowl A viruses, maintain including global HPAIcycling H5 of these subtypes viruses [1, 5]. Migratoryalong with and domestic residential poultry wild waterfowl[5–8]. Influenza maintain A viruse globals infect cycling the of intestinal these viruses tract alongof birds with such domestic that poultrywaterborne [5–8]. Influenzatransmission A virusesdominates infect their the influen intestinalza epidemiology tract of birds such[9]. Importantly, that waterborne the waterfowl– transmission dominatespoultry interface their influenza is demarcated epidemiology by shared [9]. Importantly, water in the the landscape waterfowl–poultry (Figure 1) interfaceand, therefore, is demarcated may byinfluence shared water both inspillover the landscape (transmission (Figure from1) and, wild therefore, to domestic may birds) influence and spillback both spillover (transmission (transmission from fromdomestic wild to to domestic wild birds). birds) and spillback (transmission from domestic to wild birds). Figure 1. The sharing of water resources in wetland habitat is fundamental to understanding the Figure 1. The sharing of water resources in wetland habitat is fundamental to understanding the wild wildwaterfowl–poultry waterfowl–poultry interface interface and and its itsrelevance relevance to the to the infection infection ecology ecology of ofhighly highly pathogenic pathogenic avian avian influenzainfluenza virus, virus, subtype subtype H5N1. H5N1. This This virusvirus infects,infects, and and is is shed shed by, by, the the intestinal intestinal tract tract of ofboth both waterfowl waterfowl andand poultry poultry and and thus thus the the bodies bodies of of waterwater associatedassociated with wetlands wetlands used used by by these these birds birds can can serve serve as asa a commoncommon vehicle vehicle for for waterborne waterborne transmission transmission inin processes of of both both spillover spillover and and spillback. spillback. Nevertheless,Nevertheless, the the nature nature andand distributiondistribution of th thisis interface interface remains remains unknown unknown for for many many regions regions ofof the the world. world. ForFor example,example, whether whether certain certain kinds kinds of ofwetlands wetlands are aremore more important important than others than others for the for thewaterfowl–poultry waterfowl–poultry interface, interface, and and whether whether the theinterfac interfacee operates operates differently differently at different at different densities densities of ofpoultry, are are both critical questions questions that that remain remain unanswered. unanswered. Earlier Earlier reports reports showed showed that that poultry poultry outbreaksoutbreaks of of HPAI HPAI H5N1 H5N1 over over a a 10-year 10-year periodperiod were strongly strongly associated associated with with the the distribution distribution of ofboth both surfacesurface water water and and epizootics epizootics in wildin wild waterfowl waterfowl [10 ][10] and and poultry poultry densities densities [11]. [11]. However, However, these these reports didreports not actually did not quantify actually the quantify waterfowl–poultry the waterfowl–poul interfacetry orinterface attempt or to attempt explore to the explore specific the relationship specific betweenrelationship interface between and HPAIinterface H5N1 and outbreaks. HPAI H5N1 Moreover, outbreaks. few Moreover, specific regions few specific of the worldregions have of the been theworld subject have of in-depthbeen the investigationssubject of in-depth of the investigations nature of this of interface, the nature with of this a notable interface, exception with a notable being the Qinghaiexception Lake being and the Poyang Qinghai Lake Lake regions and Poyang in China Lake [12 regions]. in China [12]. IndiaIndia provides provides critical critical winteringwintering groundsgrounds for migratory waterfowl waterfowl species, species, maintains maintains many many populationspopulations of of resident resident waterfowlwaterfowl species,species, and is is also also a a global global hotspot hotspot for for HPAI HPAI H5N1 H5N1 [7,8,13]. [7,8,13 ]. PreviousPrevious work work has has identified identified the the importance importance of surf surfaceace water water to to the the landscape landscape epidemiology epidemiology of HPAI of HPAI H5N1 epizootics in Asia more generally [13], but did not distinguish between different wetland H5N1 epizootics in Asia more generally [13], but did not distinguish between different wetland environments, which may facilitate waterfowl–poultry interface differently. Other work focused on environments, which may facilitate