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      Virus evolution and transmission in an ever more connected world

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          Abstract

          The frequency and global impact of infectious disease outbreaks, particularly those caused by emerging viruses, demonstrate the need for a better understanding of how spatial ecology and pathogen evolution jointly shape epidemic dynamics. Advances in computational techniques and the increasing availability of genetic and geospatial data are helping to address this problem, particularly when both information sources are combined. Here, we review research at the intersection of evolutionary biology, human geography and epidemiology that is working towards an integrated view of spatial incidence, host mobility and viral genetic diversity. We first discuss how empirical studies have combined viral spatial and genetic data, focusing particularly on the contribution of evolutionary analyses to epidemiology and disease control. Second, we explore the interplay between virus evolution and global dispersal in more depth for two pathogens: human influenza A virus and chikungunya virus. We discuss the opportunities for future research arising from new analyses of human transportation and trade networks, as well as the associated challenges in accessing and sharing relevant spatial and genetic data.

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          Most cited references47

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          Changing patterns of chikungunya virus: re-emergence of a zoonotic arbovirus.

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            Ecological and immunological determinants of influenza evolution.

            In pandemic and epidemic forms, influenza causes substantial, sometimes catastrophic, morbidity and mortality. Intense selection from the host immune system drives antigenic change in influenza A and B, resulting in continuous replacement of circulating strains with new variants able to re-infect hosts immune to earlier types. This 'antigenic drift' often requires a new vaccine to be formulated before each annual epidemic. However, given the high transmissibility and mutation rate of influenza, the constancy of genetic diversity within lineages over time is paradoxical. Another enigma is the replacement of existing strains during a global pandemic caused by 'antigenic shift'--the introduction of a new avian influenza A subtype into the human population. Here we explore ecological and immunological factors underlying these patterns using a mathematical model capturing both realistic epidemiological dynamics and viral evolution at the sequence level. By matching model output to phylogenetic patterns seen in sequence data collected through global surveillance, we find that short-lived strain-transcending immunity is essential to restrict viral diversity in the host population and thus to explain key aspects of drift and shift dynamics.
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              Emergence and potential for spread of Chikungunya virus in Brazil

              Background In December 2013, an outbreak of Chikungunya virus (CHIKV) caused by the Asian genotype was notified in the Caribbean. The outbreak has since spread to 38 regions in the Americas. By September 2014, the first autochthonous CHIKV infections were confirmed in Oiapoque, North Brazil, and in Feira de Santana, Northeast Brazil. Methods We compiled epidemiological and clinical data on suspected CHIKV cases in Brazil and polymerase-chain-reaction-based diagnostic was conducted on 68 serum samples from patients with symptom onset between April and September 2014. Two imported and four autochthonous cases were selected for virus propagation, RNA isolation, full-length genome sequencing, and phylogenetic analysis. We then followed CDC/PAHO guidelines to estimate the risk of establishment of CHIKV in Brazilian municipalities. Results We detected 41 CHIKV importations and 27 autochthonous cases in Brazil. Epidemiological and phylogenetic analyses indicated local transmission of the Asian CHIKV genotype in Oiapoque. Unexpectedly, we also discovered that the ECSA genotype is circulating in Feira de Santana. The presumed index case of the ECSA genotype was an individual who had recently returned from Angola and developed symptoms in Feira de Santana. We estimate that, if CHIKV becomes established in Brazil, transmission could occur in 94% of municipalities in the country and provide maps of the risk of importation of each strain of CHIKV in Brazil. Conclusions The etiological strains associated with the early-phase CHIKV outbreaks in Brazil belong to the Asian and ECSA genotypes. Continued surveillance and vector mitigation strategies are needed to reduce the future public health impact of CHIKV in the Americas. Electronic supplementary material The online version of this article (doi:10.1186/s12916-015-0348-x) contains supplementary material, which is available to authorized users.
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                Author and article information

                Journal
                Proc Biol Sci
                Proc. Biol. Sci
                RSPB
                royprsb
                Proceedings of the Royal Society B: Biological Sciences
                The Royal Society
                0962-8452
                1471-2954
                22 December 2015
                22 December 2015
                : 282
                : 1821
                : 20142878
                Affiliations
                [1 ]Department of Zoology, University of Oxford , South Parks Road, Oxford OX1 3PS, UK
                [2 ]Department of Geography and Environment, University of Southampton , Highfield, Southampton SO17 1BJ, UK
                [3 ]Fogarty International Center, National Institutes of Health , Bethesda, MA, USA
                [4 ]Flowminder Foundation , Stockholm, Sweden
                [5 ]Department of Microbiology and Immunology, Rega Institute, KU Leuven—University of Leuven , Leuven, Belgium
                Author notes

                One contribution to the special feature ‘Evolution and genetics in medicine’ Guest edited by Roy Anderson and Brian Spratt.

                An invited review to commemorate 350 years of scientific publishing at the Royal Society.

                Article
                rspb20142878
                10.1098/rspb.2014.2878
                4707738
                26702033
                2456e517-fc49-47c0-b8d3-1c01030ab4b6
                © 2015 The Authors.

                © 2015 The Authors. Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.

                History
                : 21 November 2014
                : 15 April 2015
                Funding
                Funded by: European Research Council under the European Union's Seventh Framework Programme;
                Award ID: 614725
                Funded by: NIH/NIAID;
                Award ID: U19AI089674
                Funded by: the Bill & Melinda Gates Foundation;
                Award ID: OPP110642749446
                Award ID: 1032350
                Funded by: RAPIDD program of the Science and Technology Directorate, Department of Homeland Security, and the Fogarty International Center, National Institutes of Health;
                Funded by: European Union Seventh Framework Programme;
                Award ID: 278433
                Funded by: Onderzoeksfonds KU Leuven/Research Fund KU Leuven;
                Categories
                1001
                87
                70
                200
                Special Feature
                Review Article
                Custom metadata
                December 22, 2015

                Life sciences
                virus,epidemiology,geography,evolution,phylogenetics,transmission
                Life sciences
                virus, epidemiology, geography, evolution, phylogenetics, transmission

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