1887

Abstract

Molecular studies of European classical rabies viruses (RABV) have revealed a number of geographically clustered lineages. To study the diversity of Balkan RABV, partial nucleoprotein (N) gene sequences were analysed from a unique panel of isolates ( = 210), collected from various hosts between 1972 and 2006. All of the Balkan isolates grouped within the European/Middle East Lineage, with the majority most closely related to East European strains. A number of RABV from Bosnia & Herzegovina and Montenegro, collected between 1986 and 2006, grouped with the West European strains, believed to be responsible for the rabies epizootic that spread throughout Europe in the latter half of the 20th Century. In contrast, no Serbian RABV belonged to this sublineage. However, a distinct group of Serbian fox RABV provided further evidence for the southwards wildlife-mediated movement of rabies from Hungary, Romania and Serbia into Bulgaria. To determine the optimal region for evolutionary analysis, partial, full and concatenated N-gene and glycoprotein (G) gene sequences were compared. Whilst both the divergence times and evolutionary rates were similar irrespective of genomic region, the 95 % highest probability density (HPD) limits were significantly reduced for full N-gene and concatenated NG-gene sequences compared with partial gene sequences. Bayesian coalescent analysis estimated the date of the most common recent ancestor of the Balkan RABV to be 1885 (95 % HPD, 1852–1913), and skyline plots suggested an expansion of the local viral population in 1980–1990, which coincides with the observed emergence of fox rabies in the region.

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2011-09-01
2020-01-21
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References

  1. Badrane H. , Tordo N. . ( 2001; ). Host switching in Lyssavirus history from the Chiroptera to the Carnivora orders. . J Virol 75:, 8096–8104. [CrossRef].[PubMed]
    [Google Scholar]
  2. Bourhy H. , Kissi B. , Audry L. , Smreczak M. , Sadkowska-Todys M. , Kulonen K. , Tordo N. , Zmudzinski J. F. , Holmes E. C. . ( 1999; ). Ecology and evolution of rabies virus in Europe. . J Gen Virol 80:, 2545–2557.[PubMed]
    [Google Scholar]
  3. Ćirović D. . ( 2006; ). First record of the raccoon dog (Nyctereutes procyonoides Gray, 1834) in the former Yugoslav Republic of Macedonia. . Eur J Wildl Res 52:, 136–137. [CrossRef]
    [Google Scholar]
  4. Ćirović D. , Milenković M. . ( 1999; ). Previous findings of the raccoon dog (Nyctereutes procyonoidesussuriensis Matschie, 1907) in Yugoslavia and analysis of probable paths of its immigration. . Contrib Zoogeogr Ecol East Mediterr Reg 1:, 75–82.
    [Google Scholar]
  5. David D. , Hughes G. J. , Yakobson B. A. , Davidson I. , Un H. , Aylan O. , Kuzmin I. V. , Rupprecht C. E. . ( 2007; ). Identification of novel canine rabies virus clades in the Middle East and North Africa. . J Gen Virol 88:, 967–980. [CrossRef].[PubMed]
    [Google Scholar]
  6. Davis P. L. , Rambaut A. , Bourhy H. , Holmes E. C. . ( 2007; ). The evolutionary dynamics of canid and mongoose rabies virus in Southern Africa. . Arch Virol 152:, 1251–1258. [CrossRef].[PubMed]
    [Google Scholar]
  7. Drummond A. J. , Rambaut A. . ( 2007; ). beast: Bayesian evolutionary analysis by sampling trees. . BMC Evol Biol 7:, 214. [CrossRef].[PubMed]
    [Google Scholar]
  8. Drummond A. J. , Pybus O. G. , Rambaut A. . ( 2003; ). Inference of viral evolutionary rates from molecular sequences. . Adv Parasitol 54:, 331–358. [CrossRef].[PubMed]
    [Google Scholar]
  9. Drummond A. J. , Rambaut A. , Shapiro B. , Pybus O. G. . ( 2005; ). Bayesian coalescent inference of past population dynamics from molecular sequences. . Mol Biol Evol 22:, 1185–1192. [CrossRef].[PubMed]
    [Google Scholar]
  10. Felsenstein J. . ( 1989; ). phylip – phylogeny inference package version 3.2. . Cladistics 5:, 164–166.
    [Google Scholar]
  11. Freuling C. , Selhorst T. , Bätza H. J. , Müller T. . ( 2008; ). The financial challenge of keeping a large region rabies-free–the EU example. . Dev Biol (Basel) 131:, 273–282.[PubMed]
    [Google Scholar]
  12. Hampson K. , Dushoff J. , Bingham J. , Brückner G. , Ali Y. H. , Dobson A. . ( 2007; ). Synchronous cycles of domestic dog rabies in sub-Saharan Africa and the impact of control efforts. . PNAS 104:, 7717–7722.[CrossRef]
    [Google Scholar]
  13. Hayman D. T. S. , Johnson N. , Horton D. L. , Hedge J. , Wakeley P. R. , Banyard A. C. , Zhang S. , Alhassan A. , Fooks A. R. . ( 2011; ). Evolutionary history of canine rabies in Ghana: implications for rabies control in West Africa. . PLoS Negl Trop Dis 5:, e1001.[PubMed] [CrossRef]
    [Google Scholar]
  14. Heaton P. R. , Johnstone P. , McElhinney L. M. , Cowley R. , O’Sullivan E. , Whitby J. E. . ( 1997; ). Heminested PCR assay for detection of six genotypes of rabies and rabies-related viruses. . J Clin Microbiol 35:, 2762–2766.[PubMed]
    [Google Scholar]
  15. Hughes G. J. , Orciari L. A. , Rupprecht C. E. . ( 2005; ). Evolutionary timescale of rabies virus adaptation to North American bats inferred from the substitution rate of the nucleoprotein gene. . J Gen Virol 86:, 1467–1474. [CrossRef].[PubMed]
    [Google Scholar]
  16. Johnson N. , Black C. , Smith J. , Un H. , McElhinney L. M. , Aylan O. , Fooks A. R. . ( 2003; ). Rabies emergence among foxes in Turkey. . J Wildl Dis 39:, 262–270.[PubMed] [CrossRef]
    [Google Scholar]
  17. Johnson N. , Fooks A. R. , Valtchovski R. , Müller T. . ( 2007; ). Evidence for trans-border movement of rabies by wildlife reservoirs between countries in the Balkan Peninsular. . Vet Microbiol 120:, 71–76. [CrossRef].[PubMed]
    [Google Scholar]
  18. Johnson N. , Freuling C. , Vos A. , Un H. , Valtchovski R. , Turcitu M. , Dumistrescu F. , Vuta V. , Velic R. et al. ( 2008; ). Epidemiology of rabies in southeast Europe. . Dev Biol (Basel) 131:, 189–198.[PubMed]
    [Google Scholar]
  19. Kissi B. , Tordo N. , Bourhy H. . ( 1995; ). Genetic polymorphism in the rabies virus nucleoprotein gene. . Virology 209:, 526–537. [CrossRef].[PubMed]
    [Google Scholar]
  20. Kuzmin I. V. , Botvinkin A. D. , McElhinney L. M. , Smith J. S. , Orciari L. A. , Hughes G. J. , Fooks A. R. , Rupprecht C. E. . ( 2004; ). Molecular epidemiology of terrestrial rabies in the former Soviet Union. . J Wildl Dis 40:, 617–631.[PubMed] [CrossRef]
    [Google Scholar]
  21. Lontai I. . ( 2004; ). Rabies in Hungary, Romania, Moldova and Bulgaria. . In Historical Perspective of Rabies in Europe and the Mediterranean Basin, pp. 125–127. Edited by King A. A. , Fooks A. R. , Aubert M. , Wandler A. I. . . Paris:: OIE Publications;.
    [Google Scholar]
  22. McElhinney L. M. , Marston D. , Johnson N. , Black C. , Matouch O. , Lalosevic D. , Stankov S. , Must K. , Smreczak M. et al. ( 2006; ). Molecular epidemiology of rabies viruses in Europe. . Dev Biol (Basel) 125:, 17–28.[PubMed]
    [Google Scholar]
  23. Ming P. , Yan J. , Rayner S. , Meng S. , Xu G. , Tang Q. , Wu J. , Luo J. , Yang X. . ( 2010; ). A history estimate and evolutionary analysis of rabies virus variants in China. . J Gen Virol 91:, 759–764. [CrossRef].[PubMed]
    [Google Scholar]
  24. Mutinelli F. , Stankov S. , Hristovski M. , Seimenis A. , Theoharakou H. , Vodopija I. . ( 2004;). Chapter 8. Rabies in Italy, Yugoslavia, Croatia, Bosnia, Slovenia, Macedonia Albania and Greece. . In Historical Perspective of Rabies in Europe and the Mediterranean Basin, pp. 98–118. Edited by King A. A. , Fooks A. R. , Aubert M. , Wandler A. I. . . Paris:: OIE Publications;.
    [Google Scholar]
  25. Nadin-Davis S. A. , Bingham J. . ( 2004; ). Chapter 19. Europe as a Source of Rabies for the Rest of the World. . In Perspectives of Rabies in Europe and the Mediterranean Basin, pp. 259–280. Edited by King A. A. , Fooks A. R. , Wandeler A. , Aubert M. A. . Paris:: OIE Publications;.
    [Google Scholar]
  26. Petrovic M. . ( 1987; ). Urban and sylvatic rabies in Yugoslavia. . Rabies Bulletin Europe 4:, 16–18.
    [Google Scholar]
  27. Rambaut A. . ( 2007; ) FigTree, a graphical viewer of phylogenetic trees. . http://tree.bio.ed.ac.uk/software/figtree/.
  28. Rambaut A. , Pybus O. G. , Nelson M. I. , Viboud C. , Taubenberger J. K. , Holmes E. C. . ( 2008; ). The genomic and epidemiological dynamics of human influenza A virus. . Nature 453:, 615–619. [CrossRef].[PubMed]
    [Google Scholar]
  29. Singer A. , Kauhala K. , Holmala K. , Smith G. C. . ( 2009; ). Rabies in northeastern Europe–the threat from invasive raccoon dogs. . J Wildl Dis 45:, 1121–1137.[PubMed] [CrossRef]
    [Google Scholar]
  30. Smith J. S. , Orciari L. A. , Yager P. A. , Seidel H. D. , Warner C. K. . ( 1992; ). Epidemiologic and historical relationships among 87 rabies virus isolates as determined by limited sequence analysis. . J Infect Dis 166:, 296–307. [CrossRef].[PubMed]
    [Google Scholar]
  31. Stankov S. . ( 2001; ). Typing of field rabies virus strains in FR Yugoslavia by limited sequence analysis and monoclonal antibodies. . Med Pregl 54:, 446–452.[PubMed]
    [Google Scholar]
  32. Talbi C. , Holmes E. C. , de Benedictis P. , Faye O. , Nakouné E. , Gamatié D. , Diarra A. , Elmamy B. O. , Sow A. et al. ( 2009; ). Evolutionary history and dynamics of dog rabies virus in western and central Africa. . J Gen Virol 90:, 783–791. [CrossRef].[PubMed]
    [Google Scholar]
  33. Talbi C. , Lemey P. , Suchard M. A. , Abdelatif E. , Elharrak M. , Nourlil J. , Faouzi A. , Echevarría J. E. , Vazquez Morón S. et al. ( 2010; ). Phylodynamics and human-mediated dispersal of a zoonotic virus. . PLoS Pathog 6:, e1001166. [CrossRef].[PubMed]
    [Google Scholar]
  34. Turcitu M. A. , Barboi G. , Vuta V. , Mihai I. , Boncea D. , Dumitrescu F. , Codreanu M. D. , Johnson N. , Fooks A. R. et al. ( 2010; ). Molecular epidemiology of rabies virus in Romania provides evidence for a high degree of heterogeneity and virus diversity. . Virus Res 150:, 28–33. [CrossRef].[PubMed]
    [Google Scholar]
  35. Velic R. , Sandrac V. . ( 2007; ). Rabies in Bosnia and Herzegovina 2004–2006. . Rabies Bulletin Europe 31:, 6–7.
    [Google Scholar]
  36. Wandeler A. . ( 2004; ). Epidemiology and Ecology of Fox Rabies in Europe. . In Perspectives of Rabies in Europe and the Mediterranean Basin, pp. 201–214. Edited by King A. A. , Wandeler A. , Aubert M. A. , Fooks A. R. . . Paris:: OIE Publications;.
    [Google Scholar]
  37. WHO ( 2005; ). WHO Expert Consultation on Rabies: First Report. . Geneva:: WHO;. http://www.who.int/rabies/ExpertConsultationOnRabies.pdf.
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Supplements

vol. , part 9, pp. 2171 - 2180

MCC tree of 37 FRY RABV sequences, derived from concatenated N gene and G gene sequences

Details of isolates from the Balkans and geographical regions represented in the phylogenetic analysis (N400) and evolutionary analysis

Details of isolates from the Balkans with identical sequences to representative in the phylogenetic tree (N400) [Single PDF file](135 KB)

 



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