Using phylogeographic approaches to analyse the dispersal history, velocity and direction of viral lineages - Application to rabies virus spread in Iran.


Journal

Molecular ecology
ISSN: 1365-294X
Titre abrégé: Mol Ecol
Pays: England
ID NLM: 9214478

Informations de publication

Date de publication:
09 2019
Historique:
received: 23 11 2018
revised: 04 08 2019
accepted: 05 08 2019
pubmed: 20 9 2019
medline: 12 6 2020
entrez: 20 9 2019
Statut: ppublish

Résumé

Recent years have seen the extensive use of phylogeographic approaches to unveil the dispersal history of virus epidemics. Spatially explicit reconstructions of viral spread represent valuable sources of lineage movement data that can be exploited to investigate the impact of underlying environmental layers on the dispersal of pathogens. Here, we performed phylogeographic inference and applied different post hoc approaches to analyse a new and comprehensive data set of viral genomes to elucidate the dispersal history and dynamics of rabies virus (RABV) in Iran, which have remained largely unknown. We first analysed the association between environmental factors and variations in dispersal velocity among lineages. Second, we present, test and apply a new approach to study the link between environmental conditions and the dispersal direction of lineages. The statistical performance (power of detection, false-positive rate) of this new method was assessed using simulations. We performed phylogeographic analyses of RABV genomes, allowing us to describe the large diversity of RABV in Iran and to confirm the cocirculation of several clades in the country. Overall, we estimate a relatively high lineage dispersal velocity, similar to previous estimates for dog rabies virus spread in northern Africa. Finally, we highlight a tendency for RABV lineages to spread in accessible areas associated with high human population density. Our analytical workflow illustrates how phylogeographic approaches can be used to investigate the impact of environmental factors on several aspects of viral dispersal dynamics.

Identifiants

pubmed: 31535448
doi: 10.1111/mec.15222
doi:

Banques de données

GENBANK
['KX148127', 'EF437215', 'MK760768', 'MK60770', 'MK760667', 'MK760770']

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

4335-4350

Informations de copyright

© 2019 John Wiley & Sons Ltd.

Références

Ayres, D. L., Darling, A., Zwickl, D. J., Beerli, P., Holder, M. T., Lewis, P. O., … Suchard, M. A. (2012). BEAGLE: An application programming interface and high-performance computing library for statistical phylogenetics. Systematic Biology, 61, 170-173.
Baele, G., Dellicour, S., Suchard, M. A., Lemey, P., & Vrancken, B. (2018). Recent advances in computational phylodynamics. Current Opinion in Virology, 31, 24-32.
Baltazard, M., & Ghodssi, M. (1954). Prevention of human rabies; treatment of persons bitten by rabid wolves in Iran. Bulletin of the World Health Organization, 10, 797-803.
Biek, R., Henderson, J. C., Waller, L. A., Rupprecht, C. E., & Real, L. A. (2007). A high-resolution genetic signature of demographic and spatial expansion in epizootic rabies virus. Proceedings of the National Academy of Sciences of the USA, 104, 7993-7998.
Bourhy, H., Kissi, B., Audry, L., Smreczak, M., Sadkowska-Todys, M., Kulonen, K., … Zmudzinski, J. F. (1999). Ecology and evolution of rabies virus in Europe. Journal of General Virology, 80, 2545-2557.
Bourhy, H., Nakouné, E., Hall, M., Nouvellet, P., Lepelletier, A., Talbi, C., … Rambaut, A. (2016). Revealing the micro-scale signature of endemic zoonotic disease transmission in an African urban setting. PLoS Path, 12, e1005525.
Brunker, K., Lemey, P., Marston, D. A., Fooks, A. R., Lugelo, A., Ngeleja, C., … Biek, R. (2018). Landscape attributes governing local transmission of an endemic zoonosis: Rabies virus in domestic dogs. Molecular Ecology, 27, 773-788.
Charkazi, A., Behnampour, N., Fathi, M., Esmaeili, A., Shahnazi, H., & Heshmati, H. (2013). Epidemiology of animal bite in Aq Qala city, northen of Iran. Journal of Education and Health Promotion, 2(1), 13. https://doi.org/10.4103/2277-9531.112682
Chen, J., Zou, L., Jin, Z., & Ruan, S. (2015). Modeling the geographic spread of rabies in China. PLoS Neglected Tropical Diseases, 9, e0003772.
Cliquet, F., Picard-Meyer, E., & Robardet, E. (2014). Rabies in Europe: What are the risks? Expert Review of Anti-infective Therapy, 12, 905-908. https://doi.org/10.1586/14787210.2014.921570
Criscuolo, A., & Brisse, S. (2013). AlienTrimmer: A tool to quickly and accurately trim off multiple short contaminant sequences from high-throughput sequencing reads. Genomics, 102, 500-506.
De Maio, N., Wu, C. H., O'Reilly, K. M., & Wilson, D. (2015). New routes to phylogeography: A Bayesian structured coalescent approximation. PLoS Genetics, 11, e1005421.
Dehghani, R., Sharif, A., Madani, M., Kashani, H. H., & Sharif, M. R. (2016). Factors influencing animal bites in Iran: A descriptive study. Osong Public Health and Research Perspectives, 7, 273-277.
Dellicour, S., Baele, G., Dudas, G., Faria, N. R., Pybus, O. G., Suchard, M. A., … Lemey, P. (2018). Phylodynamic assessment of intervention strategies for the West African Ebola virus outbreak. Nature Communications, 9, 2222. https://doi.org/10.1038/s41467-018-03763-2
Dellicour, S., Rose, R., Faria, N. R., Lemey, P., & Pybus, O. G. (2016). SERAPHIM: studying environmental rasters and phylogenetically informed movements. Bioinformatics, 32, 3204-3206.
Dellicour, S., Rose, R., Faria, N. R., Vieira, L. F. P., Bourhy, H., Gilbert, M., … Pybus, O. G. (2017). Using viral gene sequences to compare and explain the heterogeneous spatial dynamics of virus epidemics. Molecular Biology and Evolution, 34, 2563-2571.
Dellicour, S., Rose, R., & Pybus, O. G. (2016). Explaining the geographic spread of emerging epidemics: A framework for comparing viral phylogenies and environmental landscape data. BMC Bioinformatics, 17, 1-12. https://doi.org/10.1186/s12859-016-0924-x
Dellicour, S., Vrancken, B., Trovão, N. S.,Fargette, D., & Lemey, P. (2018). On the importance of negative controls in viral landscape phylogeography. Virus Evolution, 4, vey023.
Dijkstra, E. W. (1959). A note on two problems in connexion with graphs. Numerische Mathematik, 1, 269-271.
Dodet, B., Adjogoua, E. V., Aguemon, A. R., Amadou, O. H., Atipo, A. L., Baba, B. A., … Wateba, M. I. (2008). Fighting rabies in Africa: The Africa Rabies Expert Bureau (AfroREB). Vaccine, 26, 6295-6298.
Drummond, A. J., & Bouckaert, R. R. (2015). Bayesian evolutionary analysis with BEAST. Cambridge, UK: Cambridge University Press.
Fahrion, A. S., Taylor, L. H., Torres, G., Müller, T., Dürr, S., Knopf, L., … Abela-Ridder, B. (2017). The road to dog rabies control and elimination - What keeps us from moving faster? Frontiers in Public Health, 5, 103. https://doi.org/10.3389/fpubh.2017.00103
Farahtaj, F., Fayaz, A., Howaizi, N., Biglari, P., & Gholami, A. (2014). Human rabies in Iran. Tropical Doctor, 44, 226-229.
Feizhaddad, M. H., Kassiri, H., Lotfi, M., & Hoseini, S. S. (2014). Epidemiology and public health aspects of animal biting in shush county, Khuzestan Province, Iran. Archives of Clinical Infectious Diseases, 9, e18773.
Freuling, C. M., Hampson, K., Selhorst, T., Schröder, R., Meslin, F. X., Mettenleiter, T. C., & Müller, T. (2013). The elimination of fox rabies from Europe: Determinants of success and lessons for the future. Philosophical Transactions of the Royal Society B, 368, 20120142.
Fusaro, A., Monne, I., Salomoni, A., Angot, A., Trolese, M., Ferrè, N., …De Benedictis, P. (2013). The introduction of fox rabies into Italy (2008-2011) was due to two viral genetic groups with distinct phylogeographic patterns. Infection, Genetics and Evolution, 17, 202-209.
Gill, M. S., Lemey, P., Faria, N. R., Rambaut, A., Shapiro, B., & Suchard, M. A. (2013). Improving Bayesian population dynamics inference: A coalescent-based model for multiple loci. Molecular Biology and Evolution, 30, 713-724.
Grenfell, B. T., Bjørnstad, O. N., & Kappey, J. (2001). Travelling waves and spatial hierarchies in measles epidemics. Nature, 414, 716.
Hall, T. A. (1999). BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95-98.
Hampson, K., Coudeville, L., Lembo, T., Sambo, M., Kieffer, A., Attlan, M., … Dushoff, J. (2015). Estimating the global burden of endemic canine rabies. PLoS Neglected Tropical Diseases, 9, e0003709.
Holmes, E. C. (2004). The phylogeography of human viruses. Molecular Ecology, 13, 745-756.
Horton, D. L., McElhinney, L. M., Freuling, C. M., Marston, D. A., Banyard, A. C., Goharrriz, H., …Fooks, A. R. (2015). Complex epidemiology of a zoonotic disease in a culturally diverse region: Phylogeography of rabies virus in the Middle East. PLoS Neglected Tropical Diseases, 9, e0003569.
Hsu, A.-P., Tseng, C.-H., Barrat, J., Lee, S.-H., Shih, Y.-H., Wasniewski, M., … & Tsai, H.-J. (2017). Safety, efficacy and immunogenicity evaluation of the SAG2 oral rabies vaccine in Formosan ferret badgers. PLoS One, 12, e0184831.
Jacquot, M., Nomikou, K., Palmarini, M., Mertens, P., & Biek, R. (2017). Bluetongue virus spread in Europe is a consequence of climatic, landscape and vertebrate host factors as revealed by phylogeographic inference. Proceedings of the Royal Society B: Biological Sciences, 284, 20170919.
Janani, A. R., Fayaz, A., Simani, S., Farahtaj, F., Eslami, N., Howaizi, N., … Sabetghadam, M. (2008). Epidemiology and control of rabies in Iran. Developments in Biologicals, 131, 207-211.
Jung, M., Leye, N., Vidal, N., Fargette, D., Diop, H., Toure Kane, C., … Peeters, M. (2012). The origin and evolutionary history of HIV-1 Subtype C in Senegal. PLoS ONE, 7, e33579.
Kass, R. E., & Raftery, A. E. (1995). Bayes factors. Journal of the American Statistical Association, 90, 773-795. https://doi.org/10.1080/01621459.1995.10476572
Keeling, M. J., Woolhouse, M. E. J., Shaw, D. J., Matthews, L., Chase-Topping, M., Haydon, D. T., … Grenfell, B. T. (2001). Dynamics of the 2001 UK foot and mouth epidemic: Stochastic dispersal in a heterogeneous landscape. Science, 294, 813.
Knobel, D. L., Cleaveland, S., Coleman, P. G., Fèvre, E. M., Meltzer, M. I., Miranda, M. E. G., … Meslin, F. X. (2005). Re-evaluating the burden of rabies in Africa and Asia. Bulletin of the World Health Organization, 83, 360-368.
Kühnert, D., Wu, C. H., & Drummond, A. J. (2011). Phylogenetic and epidemic modeling of rapidly evolving infectious diseases. Infection, Genetics and Evolution, 11, 1825-1841.
Kuzmina, N. A., Lemey, P., Kuzmin, I. V., Mayes, B. C., Ellison, J. A., Orciari, L. A., … Rupprecht, C. E. (2013). The phylogeography and spatiotemporal spread of south-central skunk rabies virus. PLoS ONE, 8, e82348.
Laenen, L., Dellicour, S., Vergote, V., Nauwelaers, I., De Coster, S., Verbeeck, I., …Maes, P. (2016). Spatio-temporal analysis of Nova virus, a divergent hantavirus circulating in the European mole in Belgium. Molecular Ecology, 25, 5994-6008.
Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., … Higgins, D. G. (2007). Clustal W and Clustal X version 2.0. Bioinformatics, 23, 2947-2948.
Lembo, T. & on behalf of the Partners for Rabies Prevention (2012). The blueprint for rabies prevention and control: A novel operational toolkit for rabies elimination. PLoS Neglected Tropical Diseases, 6, e1388.
Lemey, P., Rambaut, A., Drummond, A. J., & Suchard, M. A. (2009). Bayesian phylogeography finds its roots. PLoS Computational Biology, 5, e1000520.
Lemey, P., Rambaut, A., Welch, J. J., & Suchard, M. A. (2010). Phylogeography takes a relaxed random walk in continuous space and time. Molecular Biology and Evolution, 27, 1877-1885.
Lin, Y. C., Chu, P. Y., Chang, M. Y., Hsiao, K. L., Lin, J. H., & Liu, H. F. (2016). Spatial temporal dynamics and molecular evolution of re-emerging rabies virus in Taiwan. International Journal of Molecular Sciences, 17, 392.
Marston, D. A., Horton, D. L., Nunez, J., Ellis, R. J., Orton, R. J., Johnson, N., …Fooks, A. R. (2017). Genetic analysis of a rabies virus host shift event reveals within-host viral dynamics in a new host. Virus Evolution, 3, vex038.
McElhinney, L. M., Marston, D. A., Freuling, C. M., Cragg, W., Stankov, S., Lalosević, D., …Fooks, A. R. (2011). Molecular diversity and evolutionary history of rabies virus strains circulating in the Balkans. Journal of General Virology, 92, 2171-2180.
McRae, B. H. (2006). Isolation by resistance. Evolution, 60, 1551-1561.
Müller, T., Freuling, C. M., Wysocki, P., Roumiantzeff, M., Freney, J., Mettenleiter, T. C., & Vos, A. (2015). Terrestrial rabies control in the European Union: Historical achievements and challenges ahead. Veterinary Journal, 203, 10-17.
Nadin-Davis, S. A., Simani, S., Armstrong, J., Fayaz, A., & Wandeler, A. I. (2003). Molecular and antigenic characterization of rabies viruses from Iran identifies variants with distinct epidemiological origins. Epidemiology and Infection, 131, 777-790.
Pant, G. R., Lavenir, R., Wong, F. Y. K., Certoma, A., Larrous, F., Bhatta, D. R., … Dacheux, L. (2013). Recent emergence and spread of an arctic-related phylogenetic lineage of rabies virus in Nepal. PLoS Neglected Tropical Diseases, 7, e2560.
Picot, V., Rasuli, A., Abella-Rider, A., Saadatian-Elahi, M., Aikimbayev, A., Barkia, A., … Nel, L. (2017). The Middle East and Eastern Europe rabies Expert Bureau (MEEREB) third meeting: Lyon-France (7-8 April, 2015). Journal of Infection and Public Health, 10, 695-701.
Pybus, O. G., Suchard, M. A., Lemey, P., Bernardin, F. J., Rambaut, A., Crawford, F. W., … Delwart, E. L. (2012). Unifying the spatial epidemiology and molecular evolution of emerging epidemics. Proceedings of the National Academy of Sciences of the USA, 109, 15066-15071.
Pybus, O. G., Tatem, A. J., & Lemey, P. (2015). Virus evolution and transmission in an ever more connected world. Proceedings of the Royal Society B: Biological Sciences, 282, 20142878.
Rambaut, A., Drummond, A. J., Xie, D., Baele, G., & Suchard, M. A. (2018). Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology, 67, 901-904.
Rattanavipapong, W., Thavorncharoensap, M., Youngkong, S., Genuino, A. J., Anothaisintawee, T., Chaikledkaew, U., & Meeyai, A. (2018). The impact of transmission dynamics of rabies control: Systematic review. Vaccine, in press, https://doi.org/10.1016/j.vaccine.2018.11.035
Real, L. A., & Biek, R. (2007). Spatial dynamics and genetics of infectious diseases on heterogeneous landscapes. Journal of the Royal Society Interface, 4, 935-948.
Seimenis, A. (2008). The rabies situation in the Middle East. Developments in Biologicals, 131, 43-53.
Streicker, D. G., Winternitzc, J. C., Satterfield, D. A., Condori-Condori, R. E., Broos, A., Tello, C., … Valderrama, W. (2016). Host-pathogen evolutionary signatures reveal dynamics and future invasions of vampire bat rabies. Proceedings of the National Academy of Sciences of the USA, 113, 10926-10931.
Suchard, M. A., Lemey, P., Baele, G., Ayres, D. L., & Drummond, A. J., &Rambaut, A. (2018). Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evolution, 4, vey016.
Talbi, C., Holmes, E. C., de Benedictis, P., Faye, O., Nakouné, E., Gamatié, D., … Bourhy, H. (2009). Evolutionary history and dynamics of dog rabies virus in western and central Africa. Journal of General Virology, 90, 783-791.
Talbi, C., Lemey, P., Suchard, M. A., Abdelatif, E., Elharrak, M., Jalal, N., … Bourhy, H. (2010). Phylodynamics and human-mediated dispersal of a zoonotic virus. PLoS Path, 6, e1001166.
Torres, C., Lema, C., Gury Dohmen, F., Beltran, F., Novaro, L., Russo, S., … Cisterna, D. M. (2014). Phylodynamics of vampire bat-transmitted rabies in Argentina. Molecular Ecology, 23, 2340-2352.
Troupin, C., Dacheux, L., Tanguy, M., Sabeta, C., Blanc, H., Bouchier, C., … Bourhy, H. (2016). Large-scale phylogenomic analysis reveals the complex evolutionary history of rabies virus in multiple carnivore hosts. PLoS Path, 12, e1006041.
Trovão, N. S., Baele, G., Vrancken, B., Bielejec, F., & Suchard, M. A.,Fargette, D., & Lemey, P. (2015). Host ecology determines the dispersal patterns of a plant virus. Virus Evolution, 1(1), vev016.
Un, H., Eskiizmirliler, S., Unal, N., Freuling, C. M., Johnson, N., Fooks, A. R., … Aylan, O. (2012). Oral vaccination of foxes against rabies in Turkey between 2008 and 2010. Berliner Und Munchener Tierarztliche Wochenschrift, 125, 203-208.
Vieira, L. F. P., Pereira, S. R. F. G., Carnieli, P. Jr, Tavares, L. C. B., & Kotait, I. (2013). Phylogeography of rabies virus isolated from herbivores and bats in the Espírito Santo State, Brazil. Virus Genes, 46, 330-336.
Wallace, R. M., Lai, Y., Doty, J. B., Chen, C.-C., Vora, N. M., Blanton, J. D., … Pei, K. J. C. (2018). Initial pen and field assessment of baits to use in oral rabies vaccination of Formosan ferret-badgers in response to the re-emergence of rabies in Taiwan. PLoS ONE, 13, e0189998.
WHO (2018). 0 by 30 our catalytic response. Retrieved from http://www.who.int/rabies/United_against_Rabies
Zhang, Y., Vrancken, B., Feng, Y., Dellicour, S., Yang, Q., Yang, W., … Tian, H. (2017). Cross-border spread, lineage displacement and evolutionary rate estimation of rabies virus in Yunnan Province, China. Virology Journal, 14, 102.
Zinsstag, J., Lechenne, M., Laager, M., Mindekem, R., Naïssengar, S., Oussiguéré, A., … Chitnis, N. (2017). Vaccination of dogs in an African city interrupts rabies transmission and reduces human exposure. Science Translational Medicine, 9, eaaf6984.

Auteurs

Simon Dellicour (S)

Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory for Clinical and Epidemiological Virology, KU Leuven, Leuven, Belgium.
Spatial Epidemiology Lab (SpELL), Université Libre de Bruxelles, Bruxelles, Belgium.

Cécile Troupin (C)

Unit Lyssavirus Epidemiology and Neuropathology, WHO Collaborating Centre for Reference and Research on Rabies, Institut Pasteur, Paris, France.

Fatemeh Jahanbakhsh (F)

WHO Collaborating Centre for Reference and Research on Rabies, Pasteur Institute of Iran, Tehran, Iran.

Akram Salama (A)

Department of Medicine and Infectious Diseases, Faculty of Veterinary Medicine, University of Sadat City, Sadat City, Egypt.

Siamak Massoudi (S)

Department of Environment, Wildlife Diseases Group, Wildlife Bureau, Tehran, Iran.

Madjid K Moghaddam (MK)

Department of Environment, Wildlife Diseases Group, Wildlife Bureau, Tehran, Iran.

Guy Baele (G)

Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory for Clinical and Epidemiological Virology, KU Leuven, Leuven, Belgium.

Philippe Lemey (P)

Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory for Clinical and Epidemiological Virology, KU Leuven, Leuven, Belgium.

Alireza Gholami (A)

WHO Collaborating Centre for Reference and Research on Rabies, Pasteur Institute of Iran, Tehran, Iran.

Hervé Bourhy (H)

Unit Lyssavirus Epidemiology and Neuropathology, WHO Collaborating Centre for Reference and Research on Rabies, Institut Pasteur, Paris, France.

Articles similaires

Humans Female Case-Control Studies Adult Breast Diseases
Humans Immunization, Secondary COVID-19 Vaccines COVID-19 SARS-CoV-2
1.00
Iran Environmental Monitoring Seasons Ecosystem Forests

Classifications MeSH