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Integrative molecular phylogeography in the context of infectious diseases on the human-animal interface

Published online by Cambridge University Press:  29 August 2012

REBECCA R. GRAY  and
MARCO SALEMI
REBECCA R. GRAY*
Affiliation:
Department of Zoology, University of Oxford, Tinbergen Building, South Parks Road, Oxford, UK, OX13PS
MARCO SALEMI
Affiliation:
Department of Pathology, Immunology and Laboratory Medicine and Emerging Pathogens Institute, University of Florida, Gainesville, FL, USA, 32610
*
*Corresponding author:[email protected]
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Summary

The rate of new emerging infectious diseases entering the human population has increased over the past century, with pathogens originating from animals or from products of animal origin accounting for the vast majority. Primary risk factors for the emergence and spread of emerging zoonoses include expansion and intensification of animal agriculture and long-distance live animal transport, live animal markets, bushmeat consumption and habitat destruction. Developing effective control strategies is contingent upon the ability to test causative hypotheses of disease transmission within a statistical framework. Broadly speaking, molecular phylogeography offers a framework in which specific hypotheses regarding pathogen gene flow and dispersal within an ecological context can be compared. A number of different methods has been developed for this application. Here, our intent is firstly to discuss the application of a wide variety of statistically based methods (including Bayesian reconstruction, network parsimony analysis and regression) to specific viruses (influenza, salmon anaemia virus, foot and mouth disease and Rift Valley Fever) that have been associated with animal farming/movements; and secondly to place them in the larger framework of the threat of potential zoonotic events as well as the economic and biosecurity implications of pathogen outbreaks among our animal food sources.

Keywords

Viral pathogenszoonosisanimal transportepidemic outbreaksphylogeographymolecular evolution
Type
Research Article
Information
Parasitology , Volume 139 , Issue 14: Dynamics of parasite distributions: modern analytical approaches , December 2012 , pp. 1939 - 1951
Copyright
Copyright © Cambridge University Press 2012

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References

REFERENCES

American Veterinary Medical Association (2008). One Health a new professional imperative. One Health Initiative Task Force: Final Report, July 15th 2008.Google Scholar
Anyamba, A., Chretien, J. P., Small, J., Tucker, C. J., Formenty, P. B., Richardson, J. H., Britch, S. C., Schnabel, D. C., Erickson, R. L. and Linthicum, K. J. (2009). Prediction of a Rift Valley fever outbreak. Proceedings of the National Academy of Sciences, USA 106, 955–959.CrossRefGoogle ScholarPubMed
Arzt, J., Juleff, N., Zhang, Z. and Rodriguez, L. L. (2011). The Pathogenesis of foot-and-mouth disease I: viral pathways in cattle. Transbound Emerging Diseases 58, 291–304.CrossRefGoogle ScholarPubMed
Bahl, J., Nelson, M. I., Chan, K. H., Chen, R., Vijaykrishna, D., Halpin, R. A., Stockwell, T. B., Lin, X., Wentworth, D. E., Ghedin, E., Guan, Y., Peiris, J. S., Riley, S., Rambaut, A., Holmes, E. C. and Smith, G. J. (2011). Temporally structured metapopulation dynamics and persistence of influenza A H3N2 virus in humans. Proceedings of the National Academy of Sciences, USA 108, 19359–19364.CrossRefGoogle ScholarPubMed
Biek, R. and Real, L. A. (2010). The landscape genetics of infectious disease emergence and spread. Molecular Ecology 19, 3515–3531.CrossRefGoogle ScholarPubMed
Bird, B. H., Khristova, M. L., Rollin, P. E., Ksiazek, T. G. and Nichol, S. T. (2007). Complete genome analysis of 33 ecologically and biologically diverse Rift Valley fever virus strains reveals widespread virus movement and low genetic diversity due to recent common ancestry. Journal of Virology 81, 2805–2816.CrossRefGoogle ScholarPubMed
Blake, S., Bouchard, D., Keleher, W., Opitz, M. and Nicholson, B. L. (1999). Genomic relationships of the North American isolate of infectious salmon anemia virus (ISAV) to the Norwegian strain of ISAV. Diseases of Aquatic Organisnms 35, 139–144.CrossRefGoogle Scholar
Bloomquist, E. W., Lemey, P. and Suchard, M. A. (2010). Three roads diverged? Routes to phylogeographic inference. Trends in Ecology and Evolution 25, 626–632.CrossRefGoogle ScholarPubMed
CDC (2011 a). Spread of Avian Influenza Viruses among Birds. http://www.cdc.gov/flu/avian/gen-info/spread.htmGoogle Scholar
CDC (2011 b). Types of Influenza Viruses. http://www.cdc.gov/flu/about/viruses/types.htm.Google Scholar
Chen, H., Smith, G. J. D., Zhang, S. Y., Qin, K., Wang, J., Li, K. S., Webster, R. G., Peiris, J. S. M. and Guan, Y. (2005). Avian flu: H5N1 virus outbreak in migratory water fowl. Nature 436, 191–192.CrossRefGoogle Scholar
Coker, R. J., Hunter, B. M., Rudge, J. W., Liverani, M. and Hanvoravongchai, P. (2011). Emerging infectious diseases in southeast Asia: regional challenges to control. Lancet 377, 599–609.CrossRefGoogle ScholarPubMed
Cottam, E. M., Haydon, D. T., Paton, D. J., Gloster, J., Wilesmith, J. W., Ferris, N. P., Hutchings, G. H. and King, D. P. (2006). Molecular epidemiology of the foot-and-mouth disease virus outbreak in the United Kingdom in 2001. Journal of Virology 80, 11274–11282.CrossRefGoogle ScholarPubMed
Cottam, E. M., Thébaud, G., Wadsworth, J., Gloster, J., Mansley, L., Paton, D. J., King, D. P. and Haydon, D. T. (2008 b). Integrating genetic and epidemiological data to determine transmission pathways of foot-and-mouth disease virus. Proceedings of the Royal Society B 275, 887–895.CrossRefGoogle ScholarPubMed
Cottam, E. M., Wadsworth, J., Shaw, A. E., Rowlands, R. J., Goatley, L., Maan, S., Maan, N. S., Mertens, P. P., Ebert, K., Li, Y., Ryan, E. D., Juleff, N., Ferris, N. P., Wilesmith, J. W., Haydon, D. T., King, D. P., Paton, D. J. and Knowles, N. J. (2008 a). Transmission pathways of foot-and-mouth disease virus in the United Kingdom in 2007. PLoS Pathogens 4, e1000050.CrossRefGoogle ScholarPubMed
Cottet, L., Cortez-San Martin, M., Tello, M., Olivares, E., Rivas-Aravena, A., Vallejos, E., Sandino, A. M. and Spencer, E. (2010). Bioinformatic analysis of the genome of infectious salmon anemia virus associated with outbreaks with high mortality in Chile. Journal of Virology 84, 11916–11928.CrossRefGoogle ScholarPubMed
Cottral, G. E. (1969). Persistence of foot-and-mouth disease virus in animals, their products and the environment. Bulletin de l'Office internationale des épizooties 71, 549–568.Google ScholarPubMed
Crosby, A. W. (1989). America's Forgotten Pandemic. The Influenza of 1918. Cambridge University Press, Cambridge (UK).Google Scholar
Davies, F. G. (1975). Observations on the epidemiology of Rift Valley fever in Kenya. Journal of Hygiene 75, 219–230.CrossRefGoogle ScholarPubMed
Davies, F. G., Linthicum, K. J. and James, A. D. (1985). Rainfall and epizootic Rift Valley fever. Bulletin of the World Health Organization 63, 941–943.Google ScholarPubMed
DEFRA (2002). Origin of the UK Foot and Mouth Disease epidemic in 2001. Department for Environment, Food and Rural Affairs. Available from: http://archive.defra.gov.uk/foodfarm/farmanimal/diseases/atoz/fmd/documents/fmdorigins1.pdf.Google Scholar
DEFRA (2011). ARCHIVE: Foot and Mouth Disease: 2007 outbreak. Available from: http://archive.defra.gov.uk/foodfarm/farmanimal/diseases/atoz/fmd/2007/index.htm.Google Scholar
Di Nardo, A., Knowles, N. J. and Paton, D. J. (2011). Combining livestock trade patterns with phylogenetics to help understand the spread of foot and mouth disease in sub-Saharan Africa, the Middle East and Southeast Asia. Revue Scientifique et Technique 30, 63–85.CrossRefGoogle ScholarPubMed
Drummond, A. J., Ho, S. Y., Phillips, M. J. and Rambaut, A. (2006). Relaxed phylogenetics and dating with confidence. PLoS Biology 4, e88.CrossRefGoogle ScholarPubMed
Drummond, A. J., Nicholls, G. K., Rodrigo, A. G. and Solomon, W. (2002). Estimating mutation parameters, population history and genealogy simultaneously from temporally spaced sequence data. Genetics 161, 1307–1320.CrossRefGoogle ScholarPubMed
Drummond, A. J. and Rambaut, A. (2007). BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7, 214.CrossRefGoogle ScholarPubMed
Falk, K., Aspehaug, V., Vlasak, R. and Endresen, C. (2004). Identification and characterization of viral structural proteins of infectious salmon anemia virus. Journal of Virology 78, 3063–3671.CrossRefGoogle ScholarPubMed
Fitch, W. M. (1996). The variety of human virus evolution. Molecular Phylogenetics and Evolution 5, 247–258.CrossRefGoogle ScholarPubMed
Forman, S., Le Gall, F., Belton, D., Evans, B., François, J. L., Murray, G., Sheesley, D., Vandersmissen, A. and Yoshimura, S. (2009). Moving towards the global control of foot and mouth disease: an opportunity for donors. Revue Scientifique et Technique 28, 883–896.CrossRefGoogle ScholarPubMed
Gray, R. R., Tatem, A. J., Lamers, S., Hou, W., Laeyendecker, O., Serwadda, D., Sewankambo, N., Gray, R. H., Wawer, M., Quinn, T. C., Goodenow, M. M. and Salemi, M. (2009). Spatial phylodynamics of HIV-1 epidemic emergence in east Africa. AIDS 23, F9–F17.CrossRefGoogle ScholarPubMed
Hahn, B. H., Shaw, G. M., De Cock, K. M. and Sharp, P. M. (2000). AIDS as a zoonosis: scientific and public health implications. Science 287, 607–614.CrossRefGoogle ScholarPubMed
Hay, A. J., Gregory, V., Douglas, A. R. and Lin, Y. R. (2001). The evolution of human influenza viruses. Philosophical Transactions of the Royal Society of London B: Biological Sciences 356, 1861–1870.CrossRefGoogle ScholarPubMed
Hinshaw, V. S., Webster, R. G. and Turner, B. (1980). The perpetuation of orthomyxoviruses and paramyxoviruses in Canadian waterfowl. Canadian Journal of Microbiology 26, 622–629.CrossRefGoogle ScholarPubMed
Holmes, E. C. (2008). Evolutionary history and phylogeography of human viruses. Annual Reviews in Microbiology 62, 307–328.CrossRefGoogle ScholarPubMed
Holmes, E. C. and Rambaut, A. (2004). Viral evolution and the emergence of SARS coronavirus. Philosophical Transactions of the Royal Society of London B: Biological Sciences 359, 1059–1065.CrossRefGoogle ScholarPubMed
Hoogstraal, H., Meegan, J. M., Khalil, G. M. and Adham, F. K. (1979). The Rift Valley fever epizootic in Egypt 1977–78. 2. Ecological and entomological studies. Transactions of the Royal Society of Tropical Medicine and Hygiene 73, 624–629.CrossRefGoogle ScholarPubMed
Ito, T., Couceiro, J. N., Kelm, S., Baum, L. G., Krauss, S., Castrucci, M. R., Donatelli, I., Kida, H., Paulson, J. C., Webster, R. G. and Kawaoka, Y. (1998). Molecular basis for the generation in pigs of influenza A viruses with pandemic potential. Journal of Virology 72, 7367–7373.CrossRefGoogle ScholarPubMed
Jones, K. E., Patel, N. G., Levy, M. A., Storeygard, A., Balk, D., Gittleman, J. L. and Daszak, P. (2008). Global trends in emerging infectious diseases. Nature 451, 990–993.CrossRefGoogle ScholarPubMed
Jouan, A., Coulibaly, I., Adam, F., Philippe, B., Riou, O., Leguenno, B., Christie, R., Ould Merzoug, N., Ksiazek, T. and Digoutte, J. P. (1989). Analytical study of a Rift Valley fever epidemic. Research in Virology 140, 175–186.CrossRefGoogle ScholarPubMed
Kibenge, F. S. B., Munira, K., Kibengea, M. J. T., Josepha, T. and Monekea, E. (2004). Infectious salmon anemia virus: causative agent, pathogenesis and immunity. Animal Health Research Reviews 5, 65–78.CrossRefGoogle ScholarPubMed
Kibenge, F. S., Godoy, M. G., Wang, Y., Kibenge, M. J., Gherardelli, V., Mansilla, S., Lisperger, A., Jarpa, M., Larroquete, G., Avendaño, F., Lara, M. and Gallardo, A. (2009). Infectious salmon anaemia virus (ISAV) isolated from the ISA disease outbreaks in Chile diverged from ISAV isolates from Norway around 1996 and was disseminated around 2005, based on surface glycoprotein gene sequences. Virology Journal 6, 88.CrossRefGoogle ScholarPubMed
Krkosek, M., Ford, J. S., Morton, A., Lele, S., Myers, R. A. and Lewis, M. A. (2007). Declining wild salmon populations in relation to parasites from farm salmon. Science 318, 1772–1775.CrossRefGoogle ScholarPubMed
Krossøy, B., Nilsen, F., Falk, K., Endresen, C. and Nylund, A. (2001). Phylogenetic analysis of infectious salmon anaemia virus isolates from Norway, Canada and Scotland. Diseases of Aquatic Organisms 44, 1–6.CrossRefGoogle ScholarPubMed
Lam, T. T., Zhu, H., Wang, J., Smith, D. K., Holmes, E. C., Webster, R. G., Webby, R., Peiris, J. M. and Guan, Y. (2011). Reassortment events among swine influenza A viruses in China: implications for the origin of the 2009 influenza pandemic. Journal of Virology 85, 10279–10285.CrossRefGoogle Scholar
Lemey, P., Rambaut, A., Drummond, A. J. and Suchard, M. A. (2009). Bayesian phylogeography finds its roots. PLoS Computational Biology 5, e1000520.CrossRefGoogle ScholarPubMed
Li, W., Shi, Z., Yu, M., Ren, W., Smith, C., Epstein, J. H., Wang, H., Crameri, G., Hu, Z., Zhang, H., Zhang, J., McEachern, J., Field, H., Daszak, P., Eaton, B. T., Zhang, S. and Wang, L. (2005). Bats are natural reservoirs of SARS-like coronaviruses. Science 310, 676–679.CrossRefGoogle ScholarPubMed
Lyngstad, T. M., Hjortaas, M. J., Kristoffersen, A. B., Markussen, T., Karlsen, E. T., Jonassen, C. M. and Jansen, P. A. (2011). Use of molecular epidemiology to trace transmission pathways for infectious salmon anaemia virus (ISAV) in Norwegian salmon farming. Epidemics 3, 1–11.CrossRefGoogle ScholarPubMed
Meegan, J. M. (1979). The Rift Valley fever epizootic in Egypt 1977–78. 1. Description of the epizzotic and virological studies. Transactions of the Royal Society of Tropical Medicine and Hygiene 73, 618–623.CrossRefGoogle ScholarPubMed
Morbidity and Mortality Weekly Report. (2000). Outbreak of Rift Valley Fever in Saudi Arabia. Available from: http://www.cdc.gov/mmwr/preview/mmwrhtml/mm4940a1.htmGoogle Scholar
Mundel, B. and Gear, J. (1951). Rift valley fever; I. The occurrence of human cases in Johannesburg. South African Medical Journal 25, 797–800.Google ScholarPubMed
Murray, A. G., Smith, R. J. and Stagg, R. M. (2002). Shipping and the spread of infectious salmon anemia in Scottish aquaculture. Emerging Infectious Diseases 8, 1–5.CrossRefGoogle ScholarPubMed
Nelson, M. I., Lemey, P., Tan, Y., Vincent, A., Lam, T. T., Detmer, S., Viboud, C., Suchard, M. A., Rambaut, A., Holmes, E. C., and Gramer, M. (2011). Spatial dynamics of human-origin H1 influenza a virus in North American swine. PLoS Pathogens 7, e1002077.CrossRefGoogle ScholarPubMed
Nidom, C. A., Takano, R., Yamada, S., Sakai-Tagawa, Y., Daulay, S., Aswadi, D., Suzuki, T., Suzuki, Y., Shinya, K., Iwatsuki-Horimoto, K., Muramoto, Y. and Kawaoka, Y. (2010). Influenza A (H5N1) viruses from pigs, Indonesia. Emerging Infectious Diseases 16, 1515–1523.CrossRefGoogle ScholarPubMed
Palese, P. and Shaw, M. (2007). Orthomyxoviridae: The Viruses and Their Replication. In Fields Virology, 5th Edition, (eds. Knipe, D. M. and Howley, P. M.). Lippincott Williams & Wilkins, Philadelphia, PA (USA).Google Scholar
Perry, B. D. and Rich, K. M. (2007). Povery impacts of foot-and-mouth disease and the poverty reduction implications of its control. The Veterinary Record 160, 238–241.CrossRefGoogle Scholar
Potter, C. W. (2001). A history of influenza. Journal of Applied Microbiology 91, 572–579.CrossRefGoogle ScholarPubMed
Pourrut, X., Nkoghé, D., Souris, M., Paupy, C., Paweska, J., Padilla, C., Moussavou, G. and Leroy, E. M. (2010). Rift Valley fever virus seroprevalence in human rural populations of Gabon. PLoS Neglected Tropical Diseases 4, e763.CrossRefGoogle ScholarPubMed
Rambaut, A., Pybus, O. G., Nelson, M. I., Viboud, C., Taubenberger, J. K. and Holmes, E. C. (2008). The genomic and epidemiological dynamics of human influenza A virus. Nature 453, 615–619.CrossRefGoogle ScholarPubMed
Scheel, I., Aldrin, M., Frigessi, A. and Jansen, P. A. (2007). A stochastic model for infectious salmon anemia (ISA) in Atlantic salmon farming. Journal of the Royal Society Interface 4, 699–706.CrossRefGoogle Scholar
Schneider, M. (2011). Feeding China's Pigs: Implications for the Environment, China's Smallholder Farmers and Food Security. Institute for Agriculture and Trade Policy. Available at: http://www.iatp.org/documents/feeding-china%E2%80%99s-pigs-implications-for-the-environment-china%E2%80%99s-smallholder-farmers-and-food.Google Scholar
Shields, D. A. and Mathews, K. H. (2003). Interstate Livestock Movements. USDA Economic Research Service. Available at http://www.ers.usda.gov/Publications/LDP/jun03/LDPM10801/.Google Scholar
Smith, G. J., Vijaykrishna, D., Bahl, J., Lycett, S. J., Worobey, M., Pybus, O. G., Ma, S. K., Cheung, C. L., Raghwani, J., Bhatt, S., Peiris, J. S., Guan, Y. and Rambaut, A. (2009). Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic. Nature 459, 1122–1125.CrossRefGoogle ScholarPubMed
Suchard, M. A., Weiss, R. E. and Sincheimer, J. S. (2001). Bayesian selection of continuous-time Markov chain evolutionary models. Molecular Biology and Evolution 18, 1001–1013.CrossRefGoogle ScholarPubMed
Taylor, L. H., Latham, S. M. and Woolhouse, M. E. (2001). Risk factors for human disease emergence. Philosophical Transactions of the Royal Society of London B: Biological Sciences 356, 983–989.CrossRefGoogle ScholarPubMed
Thorud, K. and Djupvik, H. O. (1988). Infectious anaemia in Atlantic salmon. Bulletin of the European Association of Fish Pathology 8, 109–111.Google Scholar
UN FAO, Fisheries and Aquaculture (2008). The State of World Fisheries and Aquaculture 2008. Available from: ftp://ftp.fao.org/docrep/fao/011/i0250e/i0250e.pdf.Google Scholar
UN FAO (2009). The State of Food and Agriculture: Livestock in the Balance. Rome (Italy). Available from http://www.fao.org/docrep/012/i0680e/i0680e00.htm.Google Scholar
UN FAO-STAT (2011). Available from: http://faostat.fao.org/site/291/default.aspx.Google Scholar
UN FAO, WHO and OIE (2004). Report of the WHO/FAO/OIE ioint consultation on emerging zoonotic diseases in collaboration with the Health Council of the Netherlands. Geneva (Switzerland). Available from http://www.oie.int/doc/en_document.php?numrec=1074503.Google Scholar
USDA (2011). Quarterly Hogs and Pigs. Available from http://www.thepigsite.com/articles/3740/usda-quarterly-hogs-and-pigs-report-december-2011-updated.Google Scholar
Webster, R. G., Bean, W. J., Gorman, O. T., Chambers, T. M. and Kawaoka, Y. (1992). Evolution and ecology of influenza A viruses. Microbiology Reviews 56, 152–179.CrossRefGoogle ScholarPubMed
Xu, X., Subbarao Cox, N. J. and Guo, Y. (1999). Genetic characterization of the pathogenic influenza A/Goose/Guangdong/1/96 (H5N1) virus: similarity of its hemagglutinin gene to those of H5N1 viruses from the 1997 outbreaks in Hong Kong. Virology 261, 15–19.CrossRefGoogle ScholarPubMed
Zhao, Z. M., Shortridge, K. F., Garica, M., Guan, Y. and Wan, X. (2008). Genotypic diversity of H5N1 highly pathogenic avian influenza viruses. Journal of General Virology 89, 2182–2193.CrossRefGoogle ScholarPubMed
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