1921
Volume 79, Issue 4
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645

Abstract

To investigate viral determinants and evolution linked to outbreak with increased severity, we examined dengue virus type 2 (DENV-2) sequences from plasma of 31 patients (14 dengue fever, 17 dengue hemorrhagic fever, DHF) continuously during the 2001 and 2002 outbreaks in southern Taiwan, in which both the total cases and proportion of DHF cases increased. Analysis of envelope (E) and full-genome sequences between viruses of the two outbreaks revealed 5 nucleotide changes in E, NS1, NS4A, and NS5 genes. None was identical to those reported in the DENV-2 outbreak in Cuba in 1997, suggesting viral determinants linked to severe outbreak are genotype dependent. Compared with previous reports of lineage turnover years apart, our findings that the 2002 viruses descended from a minor variant of the 2001 viruses in less than 6 months was novel, and may represent a mechanism of evolution of DENV from one outbreak to another.

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2008-10-01
2017-11-21
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References

  1. Lindenbach BD, Rice CM, 2001. Flaviviridae: The viruses and their replication. Knipe DM, Howley PM, eds. Fields Virology. Fourth edition. Philadelphia, PA: Lippincott Raven, 991–1041.
  2. Gubler DJ, 2002. Epidemic dengue/dengue hemorrhagic fever as a public health, social and economic problem in the 21st century. Trends Microbiol 10 : 100–103.
  3. Guzman MG, Kouri G, 2002. Dengue: an update. Lancet Infect Dis 2 : 33–42.
  4. World Health Organization, 1997. Dengue Hemorrhagic Fever, Diagnosis, Treatment and Control. Second edition. Geneva: World Health Organization.
  5. Green S, Rothman A, 2006. Immunopathological mechanisms in dengue and dengue hemorrhagic fever. Curr Opin Infect Dis 19 : 429–436.
  6. Halstead SB, 1988. Pathogenesis of dengue: challenges to molecular biology. Science 239 : 476–481.
  7. Halstead SB, O’Rourke EJ, 1977. Antibody-enhanced dengue virus infection in primate leukocytes. Nature 265 : 739–741.
  8. Morens DM, Venkateshan CN, Halstead SB, 1987. Dengue 4 virus monoclonal antibodies identify epitopes that mediate immune enhancement of dengue 2 viruses. J Gen Virol 68 : 91–98.
  9. Burke DS, Nisalak A, Johnson DE, Scott RM, 1988. A prospective study of dengue infections in Bangkok. Am J Trop Med Hyg 38 : 172–180.
  10. Guzman MG, Kouri GP, Bravo J, Soler M, Vazquez S, Morier L, 1990. Dengue hemorrhagic fever in Cuba, 1981: a retrospective seroepidemiologic study. Am J Trop Med Hyg 42 : 179–184.
  11. Sangkawibha N, Rojanasuphot S, Ahandrik S, Viriyapongse S, Jatanasen S, Salitul V, Phanthumachinda B, Halstead SB, 1984. Risk factors for dengue shock syndrome: a prospective epidemiologic in Rayong, Thailand. I. The 1980 outbreak. Am J Epidemiol 120 : 653–669.
  12. Gubler DJ, Reed D, Rosen L, Hitchcock JC, 1978. Epidemiologic, clinical and virologic observations on dengue in the kingdom of Tonga. Am J Trop Med Hyg 27 : 581–589.
  13. Messer WB, Gubler DJ, Harris E, Sivananthan K, de Silva AM, 2003. Emergence and global spread of a dengue serotype 3, subtype III virus. Emerg Infect Dis 9 : 880–889.
  14. Rico-Hesse R, Harrison LM, Salas RA, Tovar D, Nisalak A, Ramos C, Boshell J, de Mesa MT, Nogueira RM, da Rosa AT, 1997. Origins of dengue type 2 viruses associated with increased pathogenicity in the Americas. Virology 230 : 244–251.
  15. Watts D, Porter K, Putvatana R, Vasquez R, Calampa C, Hayes C, Halstead SB, 1999. Failure of secondary dengue 2 genotype I infection to cause dengue hemorrhagic fever. Lancet 354 : 1431–1434.
  16. Gubler DJ, Suharyano W, Lubis I, Eram S, Gunarso S, 1981. Epidemic dengue 3 in central Java, associated with low viremia in man. Am J Trop Med Hyg 27 : 1049–1099.
  17. Gubler DJ, Rosen L, 1977. Quantitative aspects of replication of dengue viruses in Aedes albopictus (Diptera: Culicidae) after oral and parental infection. J Med Entomol 13 : 469–472.
  18. Rosen L, 1977. The emperor’s new clothes revisited, or reflections on the pathogenesis of dengue hemorrhagic fever. Am J Trop Med Hyg 26 : 337–343.
  19. Leitmeyer KC, Vaughn DW, Watts DM, Salas R, de Chacon IV, Ramos C, Rico-Hesse R, 1999. Dengue virus structural differences that correlate with pathogenesis. J Virol 73 : 4738–4747.
  20. Cologna R, Armstrong PM, Rico-Hesse R, 2005. Selection for virulent dengue viruses occurs in human and mosquitoes. J Virol 79 : 853–859.
  21. Pryor MJ, Carr JM, Hocking H, Davidson AD, Li P, Wright PJ, 2001. Replication of dengue virus type 2 in human monocyte-derived macrophages: comparisons of isolates and recombinant viruses with substitutions at amino acid 390 in the envelope glycoprotein. Am J Trop Med Hyg 65 : 427–434.
  22. Mangada MN, Igarashi A, 1998. Molecular and in vitro analysis of eight dengue type 2 viruses isolated from patients exhibiting different disease severities. Virology 244 : 458–466.
  23. Guzman MG, Kouri G, Halstead SB, 2000. Do escape mutants explain rapid increases in dengue case-fatality rates within epidemics? Lancet 355 : 1902–1903.
  24. Guzman MG, Kouri G, Valdes L, Bravo J, Vazquez S, Halstead SB, 2002. Enhanced severity of secondary dengue-2 infection: death rates in 1981 and 1997 Cuban outbreaks. Rev Panam Salud Publica 11 : 223–227.
  25. Chao DY, Lin TH, Hwang KP, Huang JH, Liu CC, King CC, 2004. 1998 dengue hemorrhagic fever epidemic in Taiwan. Emerg Infect Dis 10 : 552–554.
  26. Wu MH, Hwang KP, Tsai JJ, Wu TS, Huang YC, King CC, 2005. Epidemiology of dengue fever/dengue hemorrhagic fever in Taiwan, 2001–2003. Taiwan J Pub Health 24 : 452–459.
  27. Rodriguez-Roche R, Alvarez M, Gritsun T, Halstead S, Kouri G, Gould EA, Guzman MG, 2005. Virus evolution during a severe dengue epidemic in Cuba, 1997. Virology 334 : 154–159.
  28. Wang WK, Chen HL, Yang CF, Hsieh SC, Juan CC, Chang SM, Yu CC, Lin LH, Huang JH, King CC, 2006. Slower rates of clearance of viral load and virus-containing immune complexes in patients with dengue hemorrhagic fever. Clin Infect Dis 43 : 1023–1030.
  29. Lanciotti RS, Calisher CH, Gubler DJ, Chang GJ, Vorndam AV, 1992. Rapid detection and typing of dengue viruses from clinical samples by using reverse transcriptase-polymerase chain reaction. J Clin Microbiol 30 : 545–551.
  30. Shu PY, Chen LK, Chang SF, Yueh YY, Chow L, Chien LJ, Lin TH, Huang JH, 2003. Comparison of capture immunoglobulin M (IgM) and IgG enzyme-linked immunosorbent assay (ELISA) and nonstructural protein NS1 serotype-specific IgG ELISA for differentiation of primary and secondary dengue virus infections. Clin Vaccine Immunol 10 : 622–630.
  31. Wang WK, Lin SR, Lee CM, King CC, Chang SC, 2002. Dengue-3 virus in plasma is a population of closely related genomes: quasispecies. J Virol 76 : 4662–4665.
  32. Kwok S, Higuchi R, 1989. Avoiding false positive with PCR. Nature 339 : 237–238.
  33. Irie K, Mohan PM, Sasaguri Y, Putnak R, Padmanabhan R, 1989. Sequence analysis of cloned dengue virus type 2 genome (New Guinea-C strain). Gene 75 : 197–211.
  34. Centers for Disease Control Taiwan, 2004. Cases of dengue hemorrhagic fever and dengue shock syndrome in Taiwan. Epidemiol Bull 20 : 46–47.
  35. Salda LTD, Parquet MDC, Matias RR, Natividad FF, Kobayashi N, Morita K, 2005. Molecular epidemiology of dengue 2 viruses in the Philippines: genotype shift and local evolution. Am J Trop Med Hyg 73 : 796–802.
  36. Twiddy SS, Farrar JJ, Chau NV, Wills B, Gould EA, Gritsun T, Lloyd G, Holmes EC, 2002. Phylogenetic relationships and differential selection pressures among genotypes of dengue-2 virus. Virology 298 : 53–72.
  37. Wang E, Ni H, Xu R, Barrett ADT, Watowich SJ, Gubler DJ, Weaver SC, 2000. Evolutionary relationships of endemic/epidemic and sylvatic dengue viruses. J Virol 74 : 3227–3234.
  38. Zhang C, Mammen MP Jr, Chinnawirotpisan P, Klungthong C, Rodpradit P, Nisalak A, Vaughn DW, Nimmannitya S, Kalayanarooj S, Holmes EC, 2006. Structure and age of genetic diversity of dengue virus type 2 in Thailand. J Gen Virol 87 : 873–883.
  39. Felsenstein J, 2005. PHYLIP (Phylogeny Inference Package) version 3.6. Program distributed by the author. Department of Genome Sciences, University of Washington, Seattle.
  40. Huelsenbeck JP, Ronquist F, 2001. MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17 : 754–755.
  41. Ronquist F, Huelsenbeck JP, 2003. MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19 : 1572–1574.
  42. Schmidt HA, Strimmer K, Vingron M, von Haeseler A, 2002. TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18 : 502–504.
  43. Nylander JAA, 2004. MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University.
  44. Kosakovsky Pond SL, Frost SDW, 2005. Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 21 : 2531–2533.
  45. Kumar S, Tamura K, Jakobsen IB, Nei M, 2001. MEGA2: molecular evolutionary genetic analysis software. Bioinformatics 17 : 1244–1245.
  46. Klungthong C, Zhang C, Mammen MP, Ubol S, Holmes EC, 2004. The molecular epidemiology of dengue virus serotype 4 in Bangkok, Thailand. Virology 329 : 168–179.
  47. Thu HM, Lowry K, Jiang L, Hlaing T, Holmes EC, Aaskov J, 2005. Lineage extinction and replacement in dengue type 1 virus populations are due to stochastic events rather than to natural selection. Virology 336 : 163–172.
  48. Lee IK, Liu JW, Yang KD, 2005. Clinical characteristics and risk factors for concurrent bacteremia in adults with dengue hemorrhagic fever. Am J Trop Med Hyg 72 : 221–226.
  49. Modis Y, Ogata S, Clements D, Harrison SC, 2004. Structure of the dengue virus envelope protein after membrane fusion. Nature 427 : 313–319.
  50. Innis BL, Thirawuth V, Hemachudha C, 1989. Identification of continuous epitopes of the envelope glycoprotein of dengue type 2 virus. Am J Trop Med Hyg 40 : 676–687.
  51. Roehrig JT, Johnson AJ, Hunt AR, Bolin RA, Chu MC, 1990. Antibodies to dengue 2 virus E-glycoprotein synthetic peptides identify abtigenic conformation. Virology 177 : 668–675.
  52. Roehrig JT, Risi PA, Brubaker JR, Hunt AR, Beaty BJ, Trent DW, Mathews JH, 1994. T-helper cell epitopes on the E-glycoprotein of dengue 2 Jamaica virus. Virology 198 : 31–38.
  53. Holmes EC, 2003. Patterns of intra- and interhost nonsynonymous variation reveal strong purifying selection in dengue virus. J Virol 77 : 11296–11298.
  54. Holmes EC, Twiddy SS, 2003. The origin, emergence and evolutionary genetics of dengue virus. Infect Genet Evol 3 : 19–28.
  55. Sittisombut N, Sistayanarain A, Cardosa MJ, Salminen M, Damrongdachakul S, Kalayanarooj S, Rojanasupot S, Supawadee J, Maneekarn N, 1997. Possible occurrence of a genetic bottle neck in dengue serotype 2 viruses between the 1980 and 1987 epidemic seasons in Bangkok, Thailand. Am J Trop Med Hyg 57 : 100–108.
  56. Wittke V, Robb TE, Thu HM, Nisalak A, Nimmannitya S, Kalayanrooj S, Vaughn DW, Endy TP, Holmes EC, Aaskov JG, 2002. Extinction and rapid evolution of strains of dengue 3 virus during an interepidemic period. Virology 301 : 148–156.
  57. Bennett SN, Holmes EC, Chirivella M, Rodriguez DM, Beltran M, Vordam V, Gubler DJ, McMillan WO, 2003. Selection-driven evolution of emergent dengue virus. Mol Biol Evol 20 : 1650–1658.
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Supplementary Data

Supplemental table 2

Supplemental table 3

Supplemental table 1

  • Received : 19 Sep 2007
  • Accepted : 14 Jun 2008

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