Reemergence of dengue virus type 4, French Antilles and French Guiana, 2004-2005.After 10 years of absence, dengue virus dengue virus n. A virus of the genus Flavivirus that is the cause of dengue. type 4 (DENV-4) has recently reemerged in Martinique, Guadeloupe, and French Guiana. Phylogenetic phy·lo·ge·net·ic adj. 1. Of or relating to phylogeny or phylogenetics. 2. Relating to or based on evolutionary development or history. analyses of strains isolated from 2004 to 2005 showed that they belong to DENV-4 genotype II, but to a different cluster than strains isolated from 1993 to 1995. ********** Dengue dengue or breakbone fever or dandy fever Infectious, disabling mosquito-borne fever. Other symptoms include extreme joint pain and stiffness, intense pain behind the eyes, a return of fever after brief pause, and a characteristic rash. is a viral disease transmitted by mosquitoes. It is caused by any of the 4 viral serotypes of dengue virus (DENV DENV Department of Environment (Canada) ), designated DENV-1, DENV-2, DENV-3, and DENV-4. DENV belongs to the genus Flavivirus and family Flaviviridae. Flaviviruses are enveloped en·vel·op tr.v. en·vel·oped, en·vel·op·ing, en·vel·ops 1. To enclose or encase completely with or as if with a covering: "Accompanying the darkness, a stillness envelops the city" , single-stranded, positive-sense RNA viruses RNA viruses, n See viruses. . The genomic RNA RNA: see nucleic acid. RNA in full ribonucleic acid One of the two main types of nucleic acid (the other being DNA), which functions in cellular protein synthesis in all living cells and replaces DNA as the carrier of genetic is [approximately equal to] 11 kb and has 10 genes coding 3 structural proteins (capsid capsid /cap·sid/ (kap´sid) the shell of protein that protects the nucleic acid of a virus; it is composed of structural units, or capsomers. cap·sid n. [C], envelope [E], and membrane [M]), and 7 nonstructural proteins (NS1, NS2a, NS2b, NS3, NS4a, NS4b, and NS5). Dengue is the predominant arthropodborne viral disease affecting humans. DENV causes a wide range of symptoms from inapparent inapparent not clearly seen. inapparent infection infection without clinical signs. or mild disease (dengue fever dengue fever (dĕng`gē, –gā), acute infectious disease caused by four closely related viruses and transmitted by the bite of the Aedes mosquito; it is also known as breakbone fever and bone-crusher disease. ) to severe forms such as dengue hemorrhagic fever hemorrhagic fever (hĕm'ərăj`ĭk), any of a group of viral diseases characterized by sudden onset, muscle and joint pain, fever, bleeding, and shock from loss of blood. (DHF DHF dihydrofolate or dihydrofolic acid. ) and dengue shock syndrome (DSS (1) (Digital Signature Standard) A National Security Administration standard for authenticating an electronic message. See RSA and digital signature. (2) (Digital Satellite S ). The disease is now endemic in >100 countries and threatens >2.5 billion people. It currently occurs in tropical areas and affects [less than or equal to] 100 million persons each year (1). Of these persons, 500,000 have DHF and [approximately equal to] 25,000, mainly children, die. The World Health Organization has estimated a 30-fold incidence increase in dengue the past 50 years (2). DENV is transmitted to humans by Stegomyia aegypti (formerly Aedes aegypti) mosquitoes. Before the 1980s, epidemic dengue was rare in the Americas because St. aegypti had been eradicated from most Central and South American countries. In the 1990s, St. aegypti had almost completely reinvaded the regions in which it was found before its eradication. Within the past 30 years, the increase in the worldwide transportation network, as well as uncontrolled population growth and urbanization, has led to larger and more frequent DENV epidemics and more cases of DHF/DSS (3). During the past 20 years, the 4 DENV serotypes have been isolated in the French departments of the Americas: Guadeloupe, Martinique, and French Guiana. Martinique and Guadeloupe are 2 Caribbean islands located in the Lesser Antilles and represent the French West Indies French West Indies: see West Indies. , and French Guiana is located southeast of the French West Indies in northern South America Northern South America is a region in the continent South America. This region has a rich range of natural resources exploited to European explorers over the past couple of centuries. Most of the most populous cities, such as Bogotá, are located temperate conditions of the Andes. between Suriname and Brazil. DENV is endemic in French Guiana. Dengue epidemics occurred in this country at 4-6-year intervals from the 1960s to the early 1990s (4). The first DHF cases were associated with a DENV-2 outbreak in 1991-1992 (5). DENV-4 was sporadically isolated between 1993 and 1995. Cocirculation of DENV-1 and DENV-2 caused outbreaks between 1996 and 1998, followed by 2 consecutive DENV-3 epidemics in 2001-2002 and 2004-2005. Martinique had 3 dengue epidemics during the past decade in a setting of sporadic transmission and seasonal peaks from July to December. These epidemics were associated with DENV-2 and DENV-4 in 1995, DENV-1 in 1997, and DENV-3 in 2001 (6). The epidemiology of DENV in Guadeloupe is similar to that in Martinique, although no data are available about previous dengue epidemics. The Study Our study reports the evolution of DENV-4 in French Guiana and the French Caribbean islands since its last detection and circulation from 1993 to 1995. We studied 8 DENV-4 strains isolated from human sera from French Guiana in 1993 and 1995 (n = 6) and in 2004 and 2005 (n = 2) (Table). We also tested 3 human serum specimens from Martinique (n = 2) and Guadeloupe (n = 1) that were positive for DENV-4 during dengue surveillance in the fourth quarter of 2004. DENV-4 infection was confirmed by using virus isolation on AP 61 cells as previously described (7). We then amplified from first-passage RNA a 1,940-bp region of the genome for the E gene and adjacent prM/M and NS 1 junctions previously described (8) to analyze the phylogenetic relationships of these strains. Each PCR PCR polymerase chain reaction. PCR abbr. polymerase chain reaction Polymerase chain reaction (PCR) product was cloned by using the TOPO TOPO Tri-N-Octylphosphine Oxide TOPO Topographic/Topography TOPO Trioctyl-Phosphine Oxide ToPo Torposten (German Military Gate Post) TOPO Tunable Optical Parametric Oscillator TA Cloning kit (Invitrogen, Paisley, UK). For each isolate, 3 clones were sequenced by Genome Express (Meylan, France). We compared our 11 sequences to the 87 DENV-4 sequences available in the GenBank database. Sequences were aligned by using MacVector version 7.2 software (Oxford Molecular Ltd., Oxford, UK). Percentage of nucleotide identity between sequences was determined for all observed differences (including insertions and deletions) and was calculated for the 1,473 nt available for all 98 sequences analyzed. Sequence comparison of strains from Martinique, Guadeloupe, and French Guiana with those reported from Asia showed that nucleotide divergence is 8%-12%. The level of nucleotide divergence was lower for sequences from the Caribbean area (maximum nucleotide divergence 2.8%). All 11 newly obtained sequences were different from each other. These sequences exhibited a 0.06%-0.47% nucleotide divergence (strains isolated in 1993 and 1995) and a 0.06%-1.22% nucleotide divergence (strains isolated in 2004 and 2005) among themselves. These strains had amino acid amino acid (əmē`nō), any one of a class of simple organic compounds containing carbon, hydrogen, oxygen, nitrogen, and in certain cases sulfur. These compounds are the building blocks of proteins. changes at position 351 in the E gene (from isoleucine isoleucine (ī'səl  `sēn), organic compound, one of the 20 amino acids commonly found in animal proteins. to valine valine (văl`ēn), organic compound, one of the 22 α-amino acids commonly found in animal proteins. Only the l-stereoisomer appears in mammalian protein. ) and position 52
in the NS1 gene (from lysine lysine (lī`sēn), organic compound, one of the 20 amino acids commonly found in animal proteins. Only the l-stereoisomer appears in mammalian protein. to arginine arginine (är`jənĭn), organic compound, one of the 20 amino acids commonly found in animal proteins. Only the l-stereoisomer participates in the biosynthesis of proteins. ), which supports their
inclusion in the modern Caribbean basin clade clade Cladus, subtype Genetics A branch of biological taxa or species that share features inherited from a common ancestor; a single phylogenetic group or line. See Inheritance, Species. (8).We conducted phylogenetic analyses on nucleotide sequences by using distance and parsimony par·si·mo·ny n. 1. Unusual or excessive frugality; extreme economy or stinginess. 2. Adoption of the simplest assumption in the formulation of a theory or in the interpretation of data, especially in accordance with the rule of methods in PAUP PAUP Phylogenetic Analysis Using Parsimony * version 4.0b8 to increase the reliability of derived tree topologies (9). We also used the neighbor-joining distance matrix algorithm with the Kimura 2 parameter (Figure) and the heuristic algorithm for the maximum parsimony analysis (data not shown). Robustness of resulting topologies was examined by using bootstrap See boot. (operating system, compiler) bootstrap - To load and initialise the operating system on a computer. Normally abbreviated to "boot". From the curious expression "to pull oneself up by one's bootstraps", one of the legendary feats of Baron von Munchhausen. analyses (10). Both neighbor-joining and parsimony algorithms underwent 1,000 iterations. [FIGURE OMITTED] The phylogenetic tree constructed with the neighbor-joining method on nucleotide sequences restricted to all American DENV-4 isolates available in GenBank (Table) is shown in the Figure. Our 11 strains segregate into 2 main clades that were identified in the 2 phylogenetic analyses from consistent topologic associations and high bootstrap values. The strains isolated from French Guiana in 1993 and 1994 clustered with strains from Suriname and Costa Rica, which were isolated at the same time, as well as with a previously reported strain from Martinique isolated in 1995. Our 5 strains isolated in 2004 and 2005 are related to a group of DENV-4 genotype II sequences isolated in the Bahamas in 1998. This finding suggests that strains circulating in French departments of the Americas in 2004 and 2005 probably evolved from strains detected in the Caribbean islands during the late 1990s. Our observations confirm that DENV-4 lineages in the Caribbean and nearby regions are grouped temporally rather than by the geographic origin of the isolates, as has been previously suggested (8). Conclusions The DEN-4 serotype serotype /se·ro·type/ (ser´o-tip) the type of a microorganism determined by its constituent antigens; a taxonomic subdivision based thereon. se·ro·type n. See serovar. v. was first reported in the Americas in 1981. At that time, isolates collected in the Americas were similar to strains collected in Southeast Asia. This lineage was designated DENV-4 genotype II (11). Since it was first detected in Dominica and the French islands of Saint Barthelemy and Saint Martin (12), this genotype has spread rapidly throughout the Caribbean and Latin America and caused DF and sporadic cases of DHF/DSS (3). DENV-4 genotype II never stopped circulating in the Caribbean region, despite its being periodically locally eliminated (8). This genotype reappeared in French departments of the Americas in 2004 after the introduction of a strain circulating in neighboring Caribbean islands, rather than by reemergence of a strain detected 10 years ago. Furthermore, this DENV-4 genotype was detected in French Guiana (October 2004) a few weeks after it was detected in Martinique (August 2004), which suggests that the strain came from the Antilles (Table). A similar phenomenon had already been observed in 1999 for the DENV-3 genotype (J. Morvan, unpub, data). This model of viral spread may be caused by cultural and economic ties between French departments, which allows gene flow through the Caribbean islands and South America as persons with viremia viremia /vi·re·mia/ (vi-re´me-ah) the presence of viruses in the blood. vi·re·mi·a n. The presence of viruses in the bloodstream. move through the region. This reflects the general pattern of dengue evolution in the Americas (13,14). Reintroduction of DENV-4 in the French Antilles and French Guiana in 2004 after a decade of absence highlights the risk for subsequent epidemics in persons with no immunity to dengue. As expected, the French Antilles had a major DENV-4 epidemic with cocirculation of DENV-2 from July 2005 to January 2006 (15). In contrast, only sporadic cases of DENV-4 infection have been observed in French Guiana since the beginning of 2005. This indicates that other factors such as mosquito density or human susceptibility, in addition to immune status of the host or silent transmission of the virus, can modulate the risk for dengue epidemics. Acknowledgments We thank Jacques Rosine, Pascal Chaud, Thierry Cardoso, Alain Blateau, and Philippe Quenel from the CIRE Antilles-Guyane for their helpful support. Sequences reported in this paper have been deposited in the GenBank database (accession nos. DQ390319-DQ390329). References (1.) Guzman MG, Kouri G. Dengue: an update. Lancet Infect Dis. 2002;2:3342. (2.) World Health Organization. Epidemic and pandemic pandemic /pan·dem·ic/ (pan-dem´ik) 1. a widespread epidemic of a disease. 2. widely epidemic. pan·dem·ic adj. Epidemic over a wide geographic area. n. alert and response: impact of dengue. [cited 2006 Sep 18]. Available from http://www.who.int/csr/disease/dengue/impact/en/index.html (3.) Gubler DJ. Dengue and dengue hemorrhagic fever. Clin Microbiol Rev. 1998; 11:480-96. (4.) Fouque F, Reynes JM, Moreau JP. Dengue in French Guiana, 1969-1993. Bull Pan Am Health Organ. 1995;29:147-55. (5.) Reynes JM, Laurent A, Deubel V, Telliam E, Moreau JE The first epidemic of dengue hemorrhagic fever in French Guiana. Am J Trop Med Hyg. 1994;51:545-53. (6.) Peyrefitte CN, Couissinier-Paris P, Mercier-Perennec V, Bessaud M, Martial J, Kenane N, et al. Genetic characterization of newly reintroduced dengue virus type 3 in Martinique (French West Indies). J Clin Microbiol. 2003;41:5195-8. (7.) Tran A, Deparis X, Dussart P, Morvan J, Rabarison P, Remy F, et al. Dengue spatial and temporal patterns, French Guiana, 2001. Emerg Infect Dis. 2004;10:615-21. (8.) Foster JE, Bennett SN, Vaughan H, Vorndam V, McMillan WO, Carrington CV. Molecular evolution and phylogeny of dengue type 4 virus in the Caribbean. Virology virology, study of viruses and their role in disease. Many viruses, such as animal RNA viruses and viruses that infect bacteria, or bacteriophages, have become useful laboratory tools in genetic studies and in work on the cellular metabolic control of gene expression . 2003;306:126-34. (9.) Swofford DL. (1998). PAUP*: phylogenetic analysis using parsimony (*and other methods), Version 4.0b8. Sunderland (MA): Sinauer Associates. (10.) Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution. 1985;39:783-91. (11.) Lanciotti RS, Gubler DJ, Trent DW. Molecular evolution and phylogeny of dengue-4 viruses. J Gen Virol. 1997;78:2279-86. (12.) Centers fur Disease Control and Prevention. Dengue type 4 infections in U.S. travelers to the Caribbean. MMWR MMWR Morbidity & Mortality Weekly Report Epidemiology A news bulletin published by the CDC, which provides epidemiologic data–eg, statistics on the incidence of AIDS, rabies, rubella, STDs and other communicable diseases, causes of mortality–eg, Morb Mortal Wkly Rep. 1981;30:249-50. (13.) Foster JE, Bennett SN, Carrington CV, Vaughan H, McMillan WO. Phylogeography and molecular evolution of dengue 2 in the Caribbean basin, 1981-2000. Virology. 2004;324:48-59. (14.) Carrington CV, Foster JE, Pybus OG, Bennett SN, Holmes EC. Invasion and maintenance of dengue virus type 2 and type 4 in the Americas. J Virol. 2005;79:14680-7. (15.) Bulletin d'alertes et de surveillance Antilles Guyane. Epidemiologie de dengue en Martinique et en Guadeloupe. Numero special: suivi des epidemies de dengue aux Antilles Guyane [cited 2005 Nov]. Available from http://www.martinique.sante.gouv.fr/documents/ accueil/cire/Basag2005-13.pdf Philippe Dussart, * Anne Lavergne, * Gisele Lagathu,([dagger]) Vincent Lacoste, * Jenny Martial, ([dagger]) Jacques Morvan, * and Raymond Cesaire([dagger]) * Institut Pasteur de la Guyane, Cayenne, French Guiana; and ([dagger])Centre Hospitalier Universitaire de Fort de France, Fort de France, Martinique, French West Indies Address for correspondence: Philippe Dussart, Centre National de Reference des Arbovirus arbovirus Any of a large group of viruses that develop in arthropods (chiefly mosquitoes and ticks). The name derives from “arthropod-borne virus.” The spheroidal virus particle is encased in a fatty membrane and contains RNA; it causes no apparent harm to the , Institut Pasteur de la Guyane, 23 Ave Pasteur, BP 6010, 97306 Cayenne CEDEX, French Guiana; email: pdussart@ pasteur-cayenne.fr Dr Dussart is a virologist virologist microbiologist specializing in virology. at the Laboratoire de Virologie, Institut Pasteur de la Guyane. He is also in charge of the Centre National de Reference des Arbovirus et Virus Influenza region Antilles Guyane. His research interests include diagnosis and epidemiology of dengue virus and other arboviruses arboviruses (ar´bōvī´r  sz),n. .
Table. Dengue virus type 4 strains used for the phylogenetic
reconstruction
Country of Year of GenBank
origin Strain isolation accession no.
French Guiana FGU-Dec-1993 1993 DQ390322
FGU-Mar-1994, 1994 DQ390325, DQ390327,
-Jun-1994, Sep-1994 DQ390329
FGU-Feb-1995, -Jun-1995 1995 DQ390324, DQ390326
FGU-Oct-2004 2004 DQ390328
FGU-Fev-2005 2005 DQ390323
Guadeloupe GUA-FWI-Dec-2004 2004 DQ390320
Martinique MAR-FWI-Aug-2004, 2004 DQ390319, DQ390321
Dec-04
Bahamas BAH 1998 A, B, C 1998 AY152364-66
Barbados BDS 1993 A, B 1993 AY152375-76
BDS 1999 1999 AY152368
Costa Rica CRA 1996 1996 AY152104
Dominica DOM 1981 1981 AY152360
Ecuador ECD 1994 1994 AY152292
El Salvador ELS 1993 1993 AY152300
Honduras HON 1991 1991 AY152379
Jamaica JAM 1981 1981 AY152389
JAM 1983 1983 AY152384
Martinique MAR-FWI 1995 1995 AY152100
Mexico MEX 1991 1991 AY152378
MEX 1995 1995 AY152304
Monserrat MON 1994 A, B, C, D 1994 AY152369-71
Puerto Rico PR 1982 M03, M05 1982 AY152336, AY152344
PR 1985 M32, M33 1985 AY152856-57
PR 1986 115 1986 AY152224
PR 1987 67, 73 1987 AY152236, AY152268
PR 1990 96 1990 AY152855
PR 1992 24, 35, 36 1992 AY152112, AY152188,
AY152208
PR 1994 81, 83 1994 AY152144, AY15148
PR 1998 13,17 1998 AY152056, AY152068
Suriname SUR 1982 A, B, C, D 1982 AY152385-88
SUR 1994 A, B, C 1994 AY152372-74
Trinidad TRI 1982 A, B 1982 AY152382-83
TRI 1984 A, B 1984 AY152380-81
TRI 1994 1994 AY152377
TRI 1999 1999 AY152367
Venezuela VEN 1995 1995 AY152092
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