The incidence of dengue fever and dengue hemorrhagic fever in Brazil experienced a significant increase since the emergence of dengue virus type-3 (DENV-3) at the early 2000s. Despite the major public health concerns, there have been very few studies of the molecular epidemiology and time-scale of this DENV lineage in Brazil. In this study, we investigated the origin and dispersion dynamics of DENV-3 genotype III in Brazil by examining a large number (n = 107) of E gene sequences sampled between 2001 and 2009 from diverse Brazilian regions. These Brazilian sequences were combined with 457 DENV-3 genotype III E gene sequences from 29 countries around the world. Our phylogenetic analysis reveals that there have been at least four introductions of the DENV-3 genotype III in Brazil, as signified by the presence of four phylogenetically distinct lineages. Three lineages (BR-I, BR-II, and BR-III) were probably imported from the Lesser Antilles (Caribbean), while the fourth one (BR-IV) was probably introduced from Colombia or Venezuela. While lineages BR-I and BR-II succeeded in getting established and disseminated in Brazil and other countries from the Southern Cone, lineages BR-III and BR-IV were only detected in one single individual each from the North region. The phylogeographic analysis indicates that DENV-3 lineages BR-I and BR-II were most likely introduced into Brazil through the Southeast and North regions around 1999 (95% HPD: 1998–2000) and 2001 (95% HPD: 2000–2002), respectively. These findings show that importation of DENV-3 lineages from the Caribbean islands into Brazil seems to be relatively frequent. Our study further suggests that the North and Southeast Brazilian regions were the most important hubs of introduction and spread of DENV-3 lineages and deserve an intense epidemiological surveillance.
References
[1]
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. doi: 10.1016/S0966-842X(01)02288-0
[2]
Gubler DJ (1998) Dengue and dengue hemorrhagic fever. Clin Microbiol Rev 11: 480–496. doi: 10.1006/pest.1998.2332
[3]
Cologna R, Armstrong PM, Rico-Hesse R (2005) Selection for virulent dengue viruses occurs in humans and mosquitoes. J Virol 79: 853–859. doi: 10.1128/JVI.79.2.853-859.2005
[4]
Rico-Hesse R (2010) Dengue virus virulence and transmission determinants. Curr Top Microbiol Immunol 338: 45–55. doi: 10.1007/978-3-642-02215-9_4
[5]
Vu TT, Holmes EC, Duong V, Nguyen TQ, Tran TH, et al. (2010) Emergence of the Asian 1 genotype of dengue virus serotype 2 in viet nam: in vivo fitness advantage and lineage replacement in South-East Asia. PLoS Negl Trop Dis 4: e757. doi: 10.1371/journal.pntd.0000757
[6]
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: 800–809. doi: 10.3201/eid0907.030038
[7]
Dash PK, Parida MM, Saxena P, Abhyankar A, Singh CP, et al. (2006) Reemergence of dengue virus type-3 (subtype-III) in India: implications for increased incidence of DHF & DSS. Virol J 3: 55. doi: 10.1186/1743-422X-3-55
[8]
Kanakaratne N, Wahala WM, Messer WB, Tissera HA, Shahani A, et al. (2009) Severe dengue epidemics in Sri Lanka, 2003–2006. Emerg Infect Dis 15: 192–199. doi: 10.3201/eid1502.080926
[9]
Dorji T, Yoon IK, Holmes EC, Wangchuk S, Tobgay T, et al. (2009) Diversity and origin of dengue virus serotypes 1, 2, and 3, Bhutan. Emerg Infect Dis 15: 1630–1632. doi: 10.3201/eid1510.090123
[10]
Franco L, Di Caro A, Carletti F, Vapalahti O, Renaudat C, et al. (2010) Recent expansion of dengue virus serotype 3 in West Africa. Euro Surveill 15.
[11]
Usuku S, Castillo L, Sugimoto C, Noguchi Y, Yogo Y, et al. (2001) Phylogenetic analysis of dengue-3 viruses prevalent in Guatemala during 1996–1998. Arch Virol 146: 1381–1390. doi: 10.1007/s007050170098
[12]
Miagostovich MP, dos Santos FB, de Simone TS, Costa EV, Filippis AM, et al. (2002) Genetic characterization of dengue virus type 3 isolates in the State of Rio de Janeiro, 2001. Braz J Med Biol Res 35: 869–872. doi: 10.1590/S0100-879X2002000800002
[13]
Peyrefitte CN, Couissinier-Paris P, Mercier-Perennec V, Bessaud M, Martial J, et al. (2003) Genetic characterization of newly reintroduced dengue virus type 3 in Martinique (French West Indies). J Clin Microbiol 41: 5195–5198. doi: 10.1128/JCM.41.11.5195-5198.2003
[14]
Peyrefitte CN, Pastorino BA, Bessaud M, Gravier P, Tock F, et al. (2005) Dengue type 3 virus, Saint Martin, 2003–2004. Emerg Infect Dis 11: 757–761. doi: 10.3201/eid1105.040959
[15]
Rodriguez-Roche R, Alvarez M, Holmes EC, Bernardo L, Kouri G, et al. (2005) Dengue virus type 3, Cuba, 2000–2002. Emerg Infect Dis 11: 773–774. doi: 10.3201/eid1105.040916
[16]
Aquino VH, Anatriello E, Goncalves PF, EV DAS, Vasconcelos PF, et al. (2006) Molecular epidemiology of dengue type 3 virus in Brazil and Paraguay, 2002–2004. Am J Trop Med Hyg 75: 710–715.
[17]
Kochel T, Aguilar P, Felices V, Comach G, Cruz C, et al. (2008) Molecular epidemiology of dengue virus type 3 in Northern South America: 2000–2005. Infect Genet Evol 8: 682–688. doi: 10.1016/j.meegid.2008.06.008
[18]
Villabona-Arenas CJ, Miranda-Esquivel DR, Jimenez RE (2009) Phylogeny of dengue virus type 3 circulating in Colombia between 2001 and 2007. Trop Med Int Health 14: 1241–1250. doi: 10.1111/j.1365-3156.2009.02339.x
[19]
Araujo JM, Nogueira RM, Schatzmayr HG, Zanotto PM, Bello G (2009) Phylogeography and evolutionary history of dengue virus type 3. Infect Genet Evol 9: 716–725. doi: 10.1016/j.meegid.2008.10.005
[20]
CDC (1995) Dengue type 3 infection–Nicaragua and Panama, October-November 1994. MMWR Morb Mortal Wkly Rep 44: 21–24.
[21]
Guzman MG, Vazquez S, Martinez E, Alvarez M, Rodriguez R, et al. (1996) [Dengue in Nicaragua, 1994: reintroduction of serotype 3 in the Americas]. Bol Oficina Sanit Panam 121: 102–110.
[22]
Ramirez A, Fajardo A, Moros Z, Gerder M, Caraballo G, et al. (2010) Evolution of dengue virus type 3 genotype III in Venezuela: diversification, rates and population dynamics. Virol J 7: 329. doi: 10.1186/1743-422X-7-329
Nogueira RM, Miagostovich MP, de Filippis AM, Pereira MA, Schatzmayr HG (2001) Dengue virus type 3 in Rio de Janeiro, Brazil. Mem Inst Oswaldo Cruz 96: 925–926. doi: 10.1590/S0074-02762001000700007
[25]
Nogueira RM, Schatzmayr HG, de Filippis AM, dos Santos FB, da Cunha RV, et al. (2005) Dengue virus type 3, Brazil, 2002. Emerg Infect Dis 11: 1376–1381. doi: 10.3201/eid1109.041043
[26]
Amarilla AA, de Almeida FT, Jorge DM, Alfonso HL, de Castro-Jorge LA, et al. (2009) Genetic diversity of the E protein of dengue type 3 virus. Virol J 6: 113. doi: 10.1186/1743-422X-6-113
[27]
Mondini A, de Moraes Bronzoni RV, Nunes SH, Chiaravalloti Neto F, Massad E, et al. (2009) Spatio-temporal tracking and phylodynamics of an urban dengue 3 outbreak in Sao Paulo, Brazil. PLoS Negl Trop Dis 3: e448. doi: 10.1371/journal.pntd.0000448
[28]
Igarashi A (1978) Isolation of a Singh's Aedes albopictus cell clone sensitive to Dengue and Chikungunya viruses. J Gen Virol 40: 531–544. doi: 10.1099/0022-1317-40-3-531
[29]
Gubler DJ, Kuno G, Sather GE, Velez M, Oliver A (1984) Mosquito cell cultures and specific monoclonal antibodies in surveillance for dengue viruses. Am J Trop Med Hyg 33: 158–165. doi: 10.1002/ps.1388
[30]
Miagostovich MP, dos Santos FB, Fumian TM, Guimaraes FR, da Costa EV, et al. (2006) Complete genetic characterization of a Brazilian dengue virus type 3 strain isolated from a fatal outcome. Mem Inst Oswaldo Cruz 101: 307–313. doi: 10.1590/S0074-02762006000300015
[31]
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25: 4876–4882. doi: 10.1093/nar/25.24.4876
[32]
Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25: 1253–1256. doi: 10.1093/molbev/msn083
[33]
Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696–704. doi: 10.1080/10635150390235520
[34]
Guindon S, Lethiec F, Duroux P, Gascuel O (2005) PHYML Online–a web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Res 33: W557–559. doi: 10.1093/nar/gki352
Rambaut A, Drummond A (2007) Tracer v1.4. Available from http://beastbioedacuk/Tracer.
[37]
Drummond AJ, Nicholls GK, Rodrigo AG, Solomon W (2002) Estimating mutation parameters, population history and genealogy simultaneously from temporally spaced sequence data. Genetics 161: 1307–1320.
[38]
Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7: 214. doi: 10.1186/1471-2148-7-214
[39]
Lemey P, Rambaut A, Drummond AJ, Suchard MA (2009) Bayesian phylogeography finds its roots. PLoS Comput Biol 5: e1000520. doi: 10.1371/journal.pcbi.1000520
[40]
Drummond AJ, Rambaut A, Shapiro B, Pybus OG (2005) Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol 22: 1185–1192. doi: 10.1093/molbev/msi103
[41]
Drummond AJ, Ho SY, Phillips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biol 4: e88. doi: 10.1371/journal.pbio.0040088
[42]
Oliveira MF, Galvao Araujo JM, Ferreira OC Jr, Ferreira DF, Lima DB, et al. (2010) Two lineages of dengue virus type 2, Brazil. Emerg Infect Dis 16: 576–578. doi: 10.3201/eid1603.090996
[43]
Romano CM, de Matos AM, Araujo ES, Villas-Boas LS, da Silva WC, et al. (2010) Characterization of Dengue virus type 2: new insights on the 2010 Brazilian epidemic. PLoS One 5: e11811. doi: 10.1371/journal.pone.0011811
[44]
Nogueira RM, Eppinghaus AL (2011) Dengue virus type 4 arrives in the state of Rio de Janeiro: a challenge for epidemiological surveillance and control. Mem Inst Oswaldo Cruz 106: 255–256.