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      Epidemiological features of influenza circulation in swine populations: A systematic review and meta-analysis

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          Abstract

          Background

          The emergence of the 2009 influenza pandemic virus with a swine origin stressed the importance of improving influenza surveillance in swine populations. The objectives of this systematic review and meta-analysis were to describe epidemiological features of swine influenza (SI) across the world and identify factors impacting swine influenza virus surveillance.

          Methods

          The systematic review followed the PRISMA guidelines. Articles published after 1990 containing data on SI on pig and herd-level seroprevalence, isolation and detection rates, and risk factors were included. Meta-regression analyses using seroprevalence and virological rates were performed.

          Results

          A total of 217 articles were included. Low avian influenza (AI) seroprevalence (means pig = 4.1%; herd = 15%) was found, showing that AIV do not readily establish themselves in swine while SIV seroprevalence was usually high across continents (influenza A means pig = 32.6–87.8%; herd = 29.3–100%). Higher pig density and number of pigs per farm were shown by the meta-regression analyses and/or the risk factor articles to be associated with higher SI seroprevalence. Lower seroprevalence levels were observed for countries with low-to-medium GDP. These results suggest that larger industrial farms could be more at risk of SIV circulation. Sampling swine with influenza-like illness (ILI) was positively associated with higher isolation rates; most studies in Europe, Latin and North America were targeting swine with ILI.

          Conclusions

          To improve understanding of SI epidemiology, standardization of the design and reporting of SI epidemiological studies is desirable. Performance of SI surveillance systems in low-to-medium GDP countries should be evaluated to rule out technical issues linked to lower observed SIV prevalence. Targeting certain swine age groups, farming systems and swine with ILI may improve the surveillance cost-effectiveness. However, focusing on pigs with ILI may bias virus detection against strains less virulent for swine but which may be important as pandemic threats.

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          Most cited references51

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          Isolation and characterization of H4N6 avian influenza viruses from pigs with pneumonia in Canada.

          In October 1999, H4N6 influenza A viruses were isolated from pigs with pneumonia on a commercial swine farm in Canada. Phylogenetic analyses of the sequences of all eight viral RNA segments demonstrated that these are wholly avian influenza viruses of the North American lineage. To our knowledge, this is the first report of interspecies transmission of an avian H4 influenza virus to domestic pigs under natural conditions.
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            Identification of H2N3 influenza A viruses from swine in the United States.

            Although viruses of each of the 16 influenza A HA subtypes are potential human pathogens, only viruses of the H1, H2, and H3 subtype are known to have been successfully established in humans. H2 influenza viruses have been absent from human circulation since 1968, and as such they pose a substantial human pandemic risk. In this report, we isolate and characterize genetically similar avian/swine virus reassortant H2N3 influenza A viruses isolated from diseased swine from two farms in the United States. These viruses contained leucine at position 226 of the H2 protein, which has been associated with increased binding affinity to the mammalian alpha2,6Gal-linked sialic acid virus receptor. Correspondingly, the H2N3 viruses were able to cause disease in experimentally infected swine and mice without prior adaptation. In addition, the swine H2N3 virus was infectious and highly transmissible in swine and ferrets. Taken together, these findings suggest that the H2N3 virus has undergone some adaptation to the mammalian host and that their spread should be very closely monitored.
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              Highly Pathogenic Avian Influenza (H5N1): Pathways of Exposure at the Animal‐Human Interface, a Systematic Review

              Background The threat posed by highly pathogenic avian influenza A H5N1 viruses to humans remains significant, given the continued occurrence of sporadic human cases (499 human cases in 15 countries) with a high case fatality rate (approximately 60%), the endemicity in poultry populations in several countries, and the potential for reassortment with the newly emerging 2009 H1N1 pandemic strain. Therefore, we review risk factors for H5N1 infection in humans. Methods and Findings Several epidemiologic studies have evaluated the risk factors associated with increased risk of H5N1 infection among humans who were exposed to H5N1 viruses. Our review shows that most H5N1 cases are attributed to exposure to sick poultry. Most cases are sporadic, while occasional limited human-to-human transmission occurs. The most commonly identified factors associated with H5N1 virus infection included exposure through contact with infected blood or bodily fluids of infected poultry via food preparation practices; touching and caring for infected poultry; consuming uncooked poultry products; exposure to H5N1 via swimming or bathing in potentially virus laden ponds; and exposure to H5N1 at live bird markets. Conclusions Research has demonstrated that despite frequent and widespread contact with poultry, transmission of the H5N1 virus from poultry to humans is rare. Available research has identified several risk factors that may be associated with infection including close direct contact with poultry and transmission via the environment. However, several important data gaps remain that limit our understanding of the epidemiology of H5N1 in humans. Although infection in humans with H5N1 remains rare, human cases continue to be reported and H5N1 is now considered endemic among poultry in parts of Asia and in Egypt, providing opportunities for additional human infections and for the acquisition of virus mutations that may lead to more efficient spread among humans and other mammalian species. Collaboration between human and animal health sectors for surveillance, case investigation, virus sharing, and risk assessment is essential to monitor for potential changes in circulating H5N1 viruses and in the epidemiology of H5N1 in order to provide the best possible chance for effective mitigation of the impact of H5N1 in both poultry and humans. Disclaimer The opinions expressed in this article are those of the authors and do not necessarily reflect those of the institutions or organizations with which they are affiliated.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                7 June 2017
                2017
                : 12
                : 6
                : e0179044
                Affiliations
                [1 ]WHO Collaborating Centre for Infectious Disease Epidemiology and Control, School of Public Health, The University of Hong Kong, Hong Kong Special Administrative Region, China
                [2 ]Animal and Integrated Risk Management Research Unit (AGIRs), French Agricultural Research Center for International Development (CIRAD), Montpellier, France
                University of Georgia, UNITED STATES
                Author notes

                Competing Interests: Dr Benjamin J. Cowling is a Section Editor for PLoS ONE. This does not alter our adherence to PLOS ONE policies on sharing data and materials.

                • Conceptualization: EB M. Peyre M. Peiris BJC.

                • Formal analysis: EB BJC.

                • Funding acquisition: M. Peyre M. Peiris BJC.

                • Investigation: EB BJC.

                • Methodology: EB M. Peyre M. Peiris BJC.

                • Resources: M. Peyre M. Peiris BJC.

                • Supervision: EB M. Peyre M. Peiris BJC.

                • Validation: EB M. Peyre M. Peiris BJC.

                • Visualization: EB.

                • Writing – original draft: EB BJC.

                • Writing – review & editing: EB M. Peyre M. Peiris BJC.

                Author information
                http://orcid.org/0000-0003-0059-6812
                Article
                PONE-D-17-02995
                10.1371/journal.pone.0179044
                5462427
                28591202
                e55fb944-94a0-4da4-8a39-cedda5624579
                © 2017 Baudon et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 23 January 2017
                : 23 May 2017
                Page count
                Figures: 6, Tables: 7, Pages: 25
                Funding
                Funded by: CIRAD
                Award Recipient :
                Funded by: Area of Excellence Scheme of the University Grants Committee
                Award ID: AoE/M-12/06
                Award Recipient :
                Funded by: Harvard Center for Communicable Disease Dynamics from the National Institute of General Medical Sciences
                Award ID: U54 GM088558
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100000002, National Institutes of Health;
                Award ID: HHSN272201400006C
                The project was funded in part by the French Agricultural Research Center for International Development (CIRAD), by the Area of Excellence Scheme of the University Grants Committee [AoE/M-12/06] of Hong Kong, the Harvard Center for Communicable Disease Dynamics from the National Institute of General Medical Sciences (grant no. U54 GM088558), and the National Institutes of Health (NIAID contract HHSN272201400006C).
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