Multiple virus lineages sharing recent common ancestry were associated with a large rift valley fever outbreak among livestock in Kenya during 2006-2007

Journal of Virology

Volumn 82, Issue 22, 2008, Pages 11152-11166

  Bird, Brian H ^a,d   Githinji, Jane W K ^c   Macharia, Joseph M ^c   Kasiiti, Jacqueline L ^c   Muriithi, Rees M ^c   Gacheru, Stephen G ^c   Musaa, Joseph O ^c   Towner, Jonathan S ^a   Reeder, Serena A ^a   Oliver, Jennifer B ^a   Stevens, Thomas L ^a   Erickson, Bobbie R ^a   Morgan, Laura T ^a   Khristova, Marina L ^b   Hartman, Amy L ^a   Comer, James A ^a   Rollin, Pierre E ^a   Ksiazek, Thomas G ^a   Nichol, Stuart T ^a  

^a CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^b CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^c Ministry of Livestock and Fisheries Development Nairobi   (Kenya)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN G; IMMUNOGLOBULIN M;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; EPIDEMIC; GENE SEQUENCE; GENETIC REASSORTMENT; GENETIC VARIABILITY; HEMORRHAGIC FEVER; KENYA; LABORATORY TEST; LIVESTOCK; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RIFT VALLEY FEVER BUNYAVIRUS; SEROLOGY; VIRUS GENOME; WILDLIFE; ANIMAL; ANIMAL DISEASE; CAMEL; CATTLE; CATTLE DISEASE; CLASSIFICATION; CLUSTER ANALYSIS; DNA SEQUENCE; DOMESTIC ANIMAL; EPIDEMIOLOGY; GENETICS; GENOTYPE; GOAT; GOAT DISEASE; HUMAN; ISOLATION AND PURIFICATION; MOLECULAR GENETICS; PHYLOGENY; SEROTYPING; SHEEP; SHEEP DISEASE; VIROLOGY;

ANIMALIA; BOS; CAMELIDAE; CAPRA HIRCUS; OVIS ARIES; RIFT VALLEY FEVER VIRUS;

ANIMALS; ANIMALS, DOMESTIC; CAMELS; CATTLE; CATTLE DISEASES; CLUSTER ANALYSIS; DISEASE OUTBREAKS; EPIDEMIOLOGY, MOLECULAR; GENOTYPE; GOAT DISEASES; GOATS; HUMANS; KENYA; MOLECULAR SEQUENCE DATA; PHYLOGENY; RIFT VALLEY FEVER; RIFT VALLEY FEVER VIRUS; SEQUENCE ANALYSIS, DNA; SEROTYPING; SHEEP; SHEEP DISEASES;

EID: 55549136054     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01519-08     Document Type: Article

References (61)

1. Anonymous. 2007. Outbreaks of Rift Valley fever in Kenya, Somalia and United Republic of Tanzania, December 2006-April 2007. Wkly. Epidemiol. Rec. 82:169-178.
2. Anyamba, A., J. P. Chretien, J. Small, C. J. Tucker, and K. J. Linthicum. 2006. Developing global climate anomalies suggest potential disease risks for 2006-2007. Int. J. Health Geogr. 5:60.
3. Beaty, B. J., E. J. Rozhon, P. Gensemer, and D. H. Bishop. 1981. Formation of reassortant bunyaviruses in dually infected mosquitoes. Virology 111:662-665.
4. Bird, B. H., C. G. Albarino, and S. T. Nichol. 2007. Rift Valley fever virus lacking NSm proteins retains high virulence in vivo and may provide a model of human delayed onset neurologic disease. Virology 362:10-15.
5. Bird, B. H., D. A. Bawiec, T. G. Ksiazek, T. R. Shoemaker, and S. T. Nichol. 2007. Highly sensitive and broadly reactive quantitative reverse transcription-PCR assay for high-throughput detection of Rift Valley fever virus. J. Clin. Microbiol. 45:3506-3513.
6. Bird, B. H., M. L. Khristova, P. E. Rollin, T. G. Ksiazek, and S. T. Nichol. 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. J. Virol. 81:2805-2816.
7. Bowen, M. D., S. G. Trappier, A. J. Sanchez, R. F. Meyer, C. S. Goldsmith, S. R. Zaki, L. M. Dunster, C. J. Peters, T. G. Ksiazek, and S. T. Nichol. 2001. A reassortant bunyavirus isolated from acute hemorrhagic fever cases in Kenya and Somalia. Virology 291:185-190.
8. Centers for Disease Control and Prevention. 1998. Rift Valley fever - East Africa 1997-1998. MMWR Morb. Mortal. Wkly. Rep. 47:261-264.
9. Centers for Disease Control and Prevention. 2007. Rift Valley fever outbreak-Kenya, November 2006-January 2007. MMWR Morb. Mortal. Wkly. Rep. 56:73-76.
10. Clement, M., D. Posada, and K. A. Crandall. 2000. TCS: a computer program to estimate gene genealogies. Mol. Ecol. 9:1657-1659.
11. Coetzer, J. A. 1982. The pathology of Rift Valley fever. II. Lesions occurring in field cases in adult cattle, calves and aborted foetuses. Onderstepoort J. Vet. Res. 49:11-17.
12. Daubney, R., J. R. Hudson, and P. C. Garnham. 1931. Enzootic hepatitis or Rift Valley fever. An undescribed virus disease of sheep cattle and man from East Africa. J. Pathol. Bacteriol. 34:545-579.
13. Drummond, A. J., and A. Rambaut. 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7:214.
14. Durand, J. P., M. Bouloy, L. Richecoeur, C. N. Peyrefitte, and H. Tolou. 2003. Rift Valley fever virus infection among French troops in Chad. Emerg. Infect. Dis. 9:751-752.
15. Easterday, B. C., M. H. McGavran, J. R. Rooney, and L. C. Murphy. 1962. The pathogenesis of Rift Valley fever in lambs. Am. J. Vet. Res. 23:470-479.
16. Enserink, M. 2008. Animal disease. Exotic disease of farm animals tests Europe's responses. Science 319:710-711.
17. European Comission. 2007. Commission regulation (EC) No. 1266/2007 of 26 October 2007 on implementing rules for Council Directive 2000/75/EC as regards the control, monitoring, surveillance and restrictions on movements of certain animals of susceptible species in relation to bluetongue, vol. L. Official Journal the European Union 283:37-52.
18. Evans, A., F. Gakuya, J. T. Paweska, M. Rostal, L. Akoolo, P. J. Van Vuren, T. Manyibe, J. M. Macharia, T. G. Ksiazek, D. R. Feikin, R. F. Breiman, and M. Kariuki Njenga. 2008. Prevalence of antibodies against Rift Valley fever virus in Kenyan wildlife. Epidemiol. Infect. 136:1261-1269.
19. Excoffier, L., and S. Schneider. 2005. Arlequin ver. 3.0: an integrated software package for population genetics analysis. Evol. Bioinformatics 2005:47-50.
20. Fu, Y. X. 1997. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915-925.
21. Galtier, N., M. Gouy, and C. Gautier. 1996. SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Comput. Appl. Biosci. 12:543-548.
22. Gerrard, S. R., B. H. Bird, C. G. Albarino, and S. T. Nichol. 2007. The NSm proteins of Rift Valley fever virus are dispensable for maturation, replication and infection. Virology 359:459-465.
23. Johnson, B. K., D. Ocheng, A. Gichogo, M. Okiro, D. Libondo, P. M. Tukei, M. Ho, M. Mugambi, G. L. Timms, and M. French. 1983. Antibodies against haemorrhagic fever viruses in Kenya populations. Trans. R. Soc. Trop. Med. Hyg. 77:731-733.
24. Katoh, K., K. Kuma, T. Miyata, and H. Toh. 2005. Improvement in the accuracy of multiple sequence alignment program MAFFT. Genome Inform. 16:22-33.
25. Kay, B. H., and R. A. Farrow. 2000. Mosquito (Diptera: Culicidae) dispersal: implications for the epidemiology of Japanese and Murray Valley encephalitis viruses in Australia. J. Med. Entomol. 37:797-801.
26. Ksiazek, T. G., A. Jouan, J. M. Meegan, B. Le Guenno, M. L. Wilson, C. J. Peters, J. P. Digoutte, M. Guillaud, N. O. Merzoug, and E. M. Touray. 1989. Rift Valley fever among domestic animals in the recent West African outbreak. Res. Virol. 140:67-77.
27. LaBeaud, A. D., Y. Ochiai, C. J. Peters, E. M. Muchiri, and C. H. King. 2007. Spectrum of Rift Valley fever virus transmission in Kenya: insights from three distinct regions. Am. J. Trop. Med. Hyg. 76:795-800.
28. Le May, N., S. Dubaele, L. Proietti De Santis, A. Billecocq, M. Bouloy, and J. M. Egly. 2004. TFIIH transcription factor, a target for the Rift Valley hemorrhagic fever virus. Cell 116:541-550.
29. Linthicum, K. J., A. Anyamba, C. J. Tucker, P. W. Kelley, M. F. Myers, and C. J. Peters. 1999. Climate and satellite indicators to forecast Rift Valley fever epidemics in Kenya. Science 285:397-400.
30. Linthicum, K. J., C. L. Bailey, F. G. Davies, A. Kairo, and T. M. Logan. 1988. The horizontal distribution of Aedes pupae and their subsequent adults within a flooded dambo in Kenya: implications for Rift Valley fever virus control. J. Am. Mosquito Control Assoc. 4:551-554.
31. Linthicum, K. J., C. L. Bailey, F. G. Davies, and C. J. Tucker. 1987. Detection of Rift Valley fever viral activity in Kenya by satellite remote sensing imagery. Science 235:1656-1659.
32. Linthicum, K. J., F. G. Davies, A. Kairo, and C. L. Bailey. 1985. Rift Valley fever virus (family Bunyaviridae, genus Phlebovirus). Isolations from Diptera collected during an inter-epizootic period in Kenya. J. Hyg. Cambridge 95:197-209.
33. Linthicum, K. J., H. F. Kaburia, F. G. Davies, and K. J. Lindqvist. 1985. A blood meal analysis of engorged mosquitoes found in Rift Valley fever epizootics area in Kenya. J. Am. Mosquito Control Assoc. 1:93-95.
34. Madani, T. A., Y. Y. Al-Mazrou, M. H. Al-Jeffri, A. A. Mishkhas, A. M. Al-Rabeah, A. M. Turkistani, M. O. Al-Sayed, A. A. Abodahish, A. S. Khan, T. G. Ksiazek, and O. Shobokshi. 2003. Rift Valley fever epidemic in Saudi Arabia: epidemiological, clinical, and laboratory characteristics. Clin. Infect. Dis. 37:1084-1092.
35. Mariner, J. C., J. Morrill, and T. G. Ksiazek. 1995. Antibodies to hemorrhagic fever viruses in domestic livestock in Niger: Rift Valley fever and Crimean-Congo hemorrhagic fever. Am. J. Trop. Med. Hyg. 53:217-221.
36. McIntosh, B. M., D. Russell, I. dos Santos, and J. H. Gear. 1980. Rift Valley fever in humans in South Africa. S. Afr. Med. J. 58:803-806.
37. Meegan, J. M., R. H. Watten, and L. W. Laughlin. 1981. Clinical experience with Rift Valley fever in humans during the 1977 egyptian epizootic. Contrib. Epidemiol. Biostatistics 3:114-123.
38. Miller, B. R., M. S. Godsey, M. B. Crabtree, H. M. Savage, Y. Al-Mazrao, M. H. Al-Jeffri, A.-M. M. Abdoon, S. M. Al-Seghayer, A. M. Al-Shahrani, and T. G. Ksiazek. 2002. Isolation and genetic characterization of Rift Valley fever virus from Aedes vexans arabiensis, Kingdom of Saudi Arabia. Emerg. Infect. Dis. 8:1492-1494.
39. Morvan, J., P. E. Rollin, S. Laventure, and J. Roux. 1992. Duration of immunoglobulin M antibodies against Rift Valley fever virus in cattle after natural infection. Trans. R. Soc. Trop. Med. Hyg. 86:675.
40. Nylander, J. A., J. C. Wilgenbusch, D. L. Warren, and D. L. Swofford. 2008. AWTY (Are We There Yet?): a system for graphical exploration of MCMC convergence in Bayesian phylogenetics. Bioinformatics 24:581-583.
41. Posada, D., and K. A. Crandall. 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817-818.
42. Ramos-Onsins, S. E., and J. Rozas. 2002. Statistical properties of new neutrality tests against population growth. Mol. Biol. Evol. 19:2092-2100.
43. Rogers, A. R., and H. Harpending. 1992. Population growth makes waves in the distribution of pairwise genetic differences. Mol. Biol. Evol. 9:552-569.
44. Ronquist, F., and J. P. Huelsenbeck. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572-1574.
45. Sall, A. A., P. M. Zanotto, O. K. Sene, H. G. Zeller, J. P. Digoutte, Y. Thiongane, and M. Bouloy. 1999. Genetic reassortment of Rift Valley fever virus in nature. J. Virol. 73:8196-8200.
46. Sall, A. A., P. M. Zanotto, P. Vialat, O. K. Sene, and M. Bouloy. 1998. Origin of 1997-98 Rift valley fever outbreak in East Africa. Lancet 352:1596-1597.
47. Schmaljohn, C. S., and J. W. Hooper. 2001. Bunyaviridae: the viruses and their replication, p. 1581-1602. In D. M. Knipe, P. M. Howley, D. E. Griffin, R. A. Lamb, M. A. Martin, B. Roizman, and S. E. Straus (ed.), Fields virology, 4th ed. Lippincott Williams & Wilkins, Philadelphia, PA.
48. Shoemaker, T., C. Boulianne, L. Pezzanite, M. Al-Qahtani, P. E. Rollin, R. Swanepoel, T. G. Ksiazek, and S. T. Nichol. 2002. Genetic analysis of viruses associated with emergence of Rift Valley fever in Saudi Arabia and Yemen, 2000-01. Emerg. Infect. Dis. 8:1415-1420.
49. Suchard, M. A., C. M. Kitchen, J. S. Sinsheimer, and R. E. Weiss. 2003. Hierarchical phylogenetic models for analyzing multipartite sequence data. Syst. Biol. 52:649-664.
50. Suchard, M. A., R. E. Weiss, and J. S. Sinsheimer. 2001. Bayesian selection of continuous-time Markov chain evolutionary models. Mol. Biol. Evol. 18:1001-1013.
51. Suzich, J. A., L. T. Kakach, and M. S. Collett. 1990. Expression strategy of a Phlebovirus: biogenesis of proteins from the Rift Valley fever virus M segment. J. Virol. 64:1549-1555.
52. Swanepoel, R. 1981. Observations on Rift Valley fever in Zimbabwe. Contrib. Epidemiol. Biostatistics 3:83-91.
53. Tajima, F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585-595.
54. Towner, J., T. Sealy, T. Ksiazek, and S. Nichol. 2007. High-throughput molecular detection of hemorrhagic fever virus threats with applications for outbreak settings. J. Infect. Dis. 2007:S202-S212.
55. Towner, J. S., M. L. Khristova, T. K. Sealy, M. J. Vincent, B. R. Erickson, D. A. Bawiec, A. L. Hartman, J. A. Comer, S. R. Zaki, U. Stroher, F. Gomes Da Silva, F. del Castillo, P. E. Rollin, T. G. Ksiazek, and S. T. Nichol. 2006. Marburgvirus genomics and association with a large hemorrhagic fever outbreak in Angola. J. Virol. 80:6497-6516.
56. Towner, J. S., P. E. Rollin, D. G. Bausch, A. Sanchez, S. M. Crary, M. Vincent, W. F. Lee, C. F. Spiropoulou, T. G. Ksiazek, M. Lukwiya, F. Kaducu, R. Downing, and S. T. Nichol. 2004. Rapid diagnosis of Ebola hemorrhagic fever by reverse transcription-PCR in an outbreak setting and assessment of patient viral load as a predictor of outcome. J. Virol. 78:4330-4341.
57. Turell, M. J., J. C. Morrill, C. A. Rossi, A. M. Gad, S. E. Cope, T. L. Clements, R. R. Arthur, L. P. Wasieloski, D. J. Dohm, D. Nash, M. M. Hassan, A. N. Hassan, Z. S. Morsy, and S. M. Presley. 2002. Isolation of West Nile and Sindbis viruses from mosquitoes collected in the Nile Valley of Egypt during an outbreak of Rift Valley fever. J. Med. Entomol. 39:248-250.
58. Wilson, A., S. Carpenter, J. Gloster, and P. Mellor. 2007. Re-emergence of bluetongue in northern Europe in 2007. Vet. Rec. 161:487-489.
59. Won, S., T. Ikegami, C. J. Peters, and S. Makino. 2006. NSm and 78-kilodalton proteins of Rift Valley fever virus are nonessential for viral replication in cell culture. J. Virol. 80:8274-8278.
60. Won, S., T. Ikegami, C. J. Peters, and S. Makino. 2007. NSm protein of Rift Valley fever virus suppresses virus-induced apoptosis. J. Virol. 81:13335-13345.
61. Woods, C. W., A. M. Karpati, T. Grein, N. McCarthy, P. Gaturuku, E. Muchiri, L. Dunster, A. Henderson, A. S. Khan, R. Swanepoel, I. Bonmarin, L. Martin, P. Mann, B. L. Smoak, M. Ryan, T. G. Ksiazek, R. R. Arthur, A. Ndikuyeze, N. N. Agata, and C. J. Peters. 2002. An outbreak of Rift Valley fever in Northeastern Kenya, 1997-98. Emerg. Infect. Dis. 8:138-144.