Abstract
Both dengue fever and its more serious clinical manifestation, dengue hemorrhagic fever, represent major public health concerns in the Americas. To understand the patterns and dynamics of virus transmission in Mexico, a country characterized by a marked increase in dengue incidence in recent years, we undertook a molecular evolutionary analysis of the largest sample of Mexican strains of dengue virus compiled to date. Our E gene data set comprises sequences sampled over a period of 27 years and representing all of the Mexican states that are endemic for dengue. Our phylogenetic analysis reveals that, for each of the four dengue viruses (DENV-1 to DENV-4), there have been multiple introductions of viral lineages in Mexico, with viruses similar to those observed throughout the Americas, but there has been strikingly little co-circulation. Rather, dengue virus evolution in Mexico is typified by frequent lineage replacement, such that only a single viral lineage dominates in a specific serotype at a specific time point. Most lineage replacement events involve members of the same viral genotype, although a replacement event involving different genotypes was observed with DENV-2, and viral lineages that are new to Mexico are described for DENV-1, DENV-3 and DENV-4.
Similar content being viewed by others
References
Armstrong PM, Rico-Hesse R (2001) Differential susceptibility of Aedes aegypti to infection by the American and Southeast Asian genotypes of dengue type 2 virus. Vector Borne Zoonotic Dis 1:159–168
Bennett SN, Holmes EC, Chirivella M, Rodriguez DM, Beltran M, Vorndam V, Gubler DJ, McMillan WO (2003) Selection-driven evolution of emergent dengue virus. Mol Biol Evol 20:1650–1658
Bennett SN, Holmes EC, Chirivella M, Rodriguez DM, Beltran M, Vorndam V, Gubler DJ, McMillan WO (2006) Molecular evolution of dengue 2 virus in Puerto Rico: positive selection in the viral envelope accompanies clade reintroduction. J Gen Virol 87:885–893
Brunkard JM, Robles López JL, Ramirez J, Cifuentes E, Rothenberg SJ, Hunsperger EA, Moore CG, Brussolo RM, Villarreal NA, Haddad BM (2007) Dengue fever seroprevalence and risk factors, Texas-Mexico border, 2004. Emerg Infect Dis 13:1477–1483
Cisneros A, Díaz-Badillo A, Cruz-Martínez G, Tovar R, Ramírez-Palacios LR, Jiménez-Rojas F, Beaty B, Black WC 4th, de Lourdes Muñoz M (2006) Dengue 2 genotypes in the state of Oaxaca, Mexico. Arch Virol 151:113–125
Cologna R, Armstrong PM, Rico-Hesse R (2005) Selection for virulent dengue viruses occurs in humans and mosquitoes. J Virol 79:853–859
Cologna R, Rico-Hesse R (2003) American genotype structures decrease dengue virus output from human monocytes and dendritic cells. J Virol 77:3929–3938
Díaz FJ, Black WC 4th, Farfán-Ale JA, Loroño-Pino MA, Olson KE, Beaty BJ (2006) Dengue virus circulation and evolution in Mexico: a phylogenetic perspective. Arch Med Res 37:760–773
Díaz FJ, Farfán-Ale JA, Olson KE, Loroño-Pino MA, Gubler DJ, Blair CD, Black WC, Beaty BJ 4th (2002) Genetic variation within the premembrane coding region of dengue viruses from the Yucatan peninsula of Mexico. Am J Trop Med Hyg 67:93–101
Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214
Foster JE, Bennett SN, Vaughan H, Vorndam V, McMillan WO, Carrington CVF (2003) Molecular evolution and phylogeny of dengue type 4 virus in the Caribbean. Virology 306:126–134
Goncalvez AP, Escalante AA, Pujol FH, Ludert JE, Tovar D, Salas RA, Liprandi F (2002) Diversity and evolution of the envelope gene of dengue virus type 1. Virology 303:110–119
Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Mol Biol Evol 52:696–704
Günther J, Ramírez-Palacio LR, Pérez-Ishiwara DG, Salas-Benito JS (2009) Distribution of dengue cases in the state of Oaxaca, Mexico, during the period 2004–2006. J Clin Virol 45:218–222
Holmes EC (2009) The evolution and emergence of RNA viruses. In: Harvey PH, May RM (eds) Oxford series in ecology and evolution (OSEE). Oxford University Press, Oxford
Holmes EC, Twiddy SS (2003) The origin, emergence and evolutionary genetics of dengue virus. Infect Genet Evol 3:19–28
Johansson MA, Cummings DA, Glass GE (2009) Multiyear climate variability and dengue: El Niño southern oscillation, weather, and dengue incidence in Puerto Rico, Mexico, and Thailand: a longitudinal data analysis. PLoS Med 6:e1000168
Lanciotti RS, Gubler DJ, Trent DW (1997) Molecular evolution and phylogeny of dengue-4 viruses. J Gen Virol 78:2279–2286
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
Loroño-Pino MA, Cropp CB, Farfán JA, Vorndam AV, Rodríguez-Angulo EM, Rosado-Paredes EP, Flores-Flores LF, Beaty BJ, Gubler DJ (1999) Common occurrence of concurrent infections by multiple dengue virus serotypes. Am J Trop Med Hyg 61:725–730
Loroño-Pino MA, Farfán-Ale JA, Rosado-Paredes EP, Kuno G, Gubler DJ (1993) Epidemic dengue 4 in the Yucatán, Mexico, 1984. Rev Inst Med Trop Sao Paulo 35:449–455
Loroño-Pino MA, Farfán-Ale JA, Zapata-Peraza AL, Rosado-Paredes EP, Flores-Flores LF, García-Rejón JE, Díaz FJ, Blitvich BJ, Andrade-Narváez M, Jiménez-Ríos E, Blair CD, Olson KE, Black WC, Beaty BJ 4th (2004) Introduction of the American/Asian genotype of dengue 2 virus into the Yucatan State of Mexico. Am J Trop Med Hyg 71:485–492
Lozano-Fuentes S, Fernandez-Salas I, de Lourdes Muñoz M, Garcia-Rejon J, Olson KE, Beaty BJ, Black WC 4th (2009) The Neovolcanic axis is a barrier to gene flow among Aedes aegypti populations in Mexico that differ in vector competence for dengue 2 virus. PLoS Negl Trop Dis 3:e468
Mota J, Ramos-Castañeda J, Rico-Hesse R, Ramos C (2002) Phylogenetic analysis of the envelope protein (domain III) of dengue 4 viruses. Salud Publica Mex 44:228–236
Perez-Ramirez G, Diaz-Badillo A, Camacho-Nuez M, Cisneros A, de Lourdes Muñoz M (2009) Multiple recombinants in two dengue virus, serotype-2 isolates from patients from Oaxaca, Mexico. BMC Microbiol 9:260
Ramos MM, Mohammed H, Zielinski-Gutierrez E, Hayden MH, Lopez JL, Fournier M, Trujillo AR, Burton R, Brunkard JM, Anaya-Lopez L, Banicki AA, Morales PK, Smith B, Muñoz JL, Waterman SH, Dengue Serosurvey Working Group (2008) Epidemic dengue and dengue hemorrhagic fever at the Texas-Mexico border: results of a household-based seroepidemiologic survey, December 2005. Am J Trop Med Hyg 78:364–369
Rico-Hesse R (2003) Microevolution and virulence of dengue viruses. Adv Virus Res 59:315–341
Rico-Hesse R, Harrison LM, Salas RA, Tovar D, Nisalak A, Ramos C, Boshell J, de Mesa MTR, Nogueira RMR, da Rosa AT (1997) Origins of dengue type 2 viruses associated with increased pathogenicity in the Americas. Virology 230:244–251
Roca Y, Baronti C, Revollo RJ, Cook S, Loayza R, Ninove L, Fernandez RT, Flores JV, Herve JP, de Lamballerie X (2009) Molecular epidemiological analysis of dengue fever in Bolivia from 1998 to 2008. Vector Borne Zoonotic Dis 9:337–344
Ruiz BH, Sánchez I, Ortega G, López I, Rosales L, Medina G (2000) Phylogenetic comparison of the DEN-2 Mexican isolate with other flaviviruses. Intervirology 43:48–54
Shapiro B, Rambaut A, Drummond AJ (2006) Choosing appropriate substitution models for the phylogenetic analysis of protein-coding sequences. Mol Biol Evol 23:7–9
Sittisombut N, Sistayanarain A, Cardosa MJ, Salminen M, Damrongdachakul S, Kalayanarooj S, Rojanasuphot S, Supawadee J, Maneekarn N (1997) Possible occurrence of a genetic bottleneck in dengue serotype 2 viruses between the 1980 and 1987 epidemic seasons in Bangkok, Thailand. Am J Trop Hyg Med 57:100–108
Tapia-Conyer R, Méndez-Galván JF, Gallardo-Rincón H (2009) The growing burden of dengue in Latin America. J Clin Virol 46(Suppl 2):S3–S6
Twiddy SS, Holmes EC, Rambaut A (2003) Inferring the rate and time-scale of dengue virus evolution. Mol Biol Evol 20:122–129
Wittke V, Robb TE, Thu HM, Nimmannitya S, Kalayanrooj S, Vaughn DW, Endy TP, Holmes EC, Aaskov JG (2002) Extinction and rapid emergence of strains of dengue 3 virus during an interepidemic period. Virology 301:148–156
Zhang C, Mammen MP Jr, Chinnawirotpisan P, Klungthong C, Rodpradit P, Monkongdee P, Nimmannitya S, Kalayanarooj S, Holmes EC (2005) Clade replacements in dengue virus serotypes 1 and 3 are associated with changing serotype prevalence. J Virol 79:15123–15130
Acknowledgments
The authors wish to thank Ms. Silvia Tenorio-Salgado for technical assistance. This work was supported by a grant FOSSIS-CONACYT SALUD-2005-01-13852 to JRC.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Carrillo-Valenzo, E., Danis-Lozano, R., Velasco-Hernández, J.X. et al. Evolution of dengue virus in Mexico is characterized by frequent lineage replacement. Arch Virol 155, 1401–1412 (2010). https://doi.org/10.1007/s00705-010-0721-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00705-010-0721-1