Vector competence of the Aedes aegypti population from Santiago Island, Cape Verde, to different serotypes of dengue virus

Particle and Fibre Toxicology

Constância Flávia Junqueira Ayres²  Lara Ferrero Gómez³  Hélio Daniel Ribeiro Rocha³  Maria Lidia da Cruz Brito³  Danilo de Carvalho-Leandro¹  Duschinka Ribeiro Duarte Guedes²  Claudia Maria Fontes Oliveira²  Maria Alice Varjal de Melo Santos²  Aires Januário Fernandes da Moura³ 

[1] Departamento de Zoologia, Universidade Federal de Pernambuco (UFPE), Programa de Pós-graduação em Biologia Animal, Recife, Brasil;Departamento de Entomologia, Centro de Pesquisas Aggeu Magalhães (CPqAM), Fundação Oswaldo Cruz- PE, Brasil;Unidade de Ciências da Natureza, da Vida e do Ambiente, Universidade Jean Piaget, Cape Verde

关键词: Cape Verde;    NS1 antigen;    Vector;    RT-PCR;    Dengue;   

Others  :  1132151
DOI  :  10.1186/s13071-015-0706-8

 received in 2014-08-12, accepted in 2015-01-30,  发布年份 2015

【 摘 要 】

Background

Dengue is an arboviral disease caused by dengue virus (DENV), whose main vectors are the mosquitoes Aedes aegypti and Aedes albopictus. A. aegypti is the only DENV vector in Cape Verde, an African country that suffered its first outbreak of dengue in 2009. However, little is known about the variation in the level of vector competence of this mosquito population to the different DENV serotypes. This study aimed to evaluate the vector competence of A. aegypti from the island of Santiago, Cape Verde, to four DENV serotypes and to detect DENV vertical transmission.

Methods

Mosquitoes were fed on blood containing DENV serotypes and were dissected at 7, 14 and 21 days post-infection (dpi) to detect the virus in the midgut, head and salivary glands (SG) using RT-PCR. Additionally, the number of copies of viral RNA present in the SG was determined by qRT-PCR. Furthermore, eggs were collected in the field and adult mosquitoes obtained were analyzed by RT-PCR and the platelia dengue NS1 antigen kit to detect transovarial transmission.

Results

High rates of SG infection were observed for DENV-2 and DENV-3 whereas for DENV-1, viral RNA was only detected in the midgut and head. DENV-4 did not spread to the head or SG, maintaining the infection only in the midgut. The number of viral RNA copies in the SG did not vary significantly between DENV-2 and DENV-3 or among the different periods of incubation and the various titers of DENV tested. With respect to DENV surveillance in mosquitoes obtained from the eggs collected in the field, no samples were positive.

Conclusion

Although no DENV positive samples were collected from the field in 2014, it is important to highlight that the A. aegypti population from Santiago Islands exhibited different degrees of susceptibility to DENV serotypes. This population showed a high vector competence for DENV-2 and DENV-3 strains and a low susceptibility to DENV-1 and DENV-4. Viral RNA copies in the SG remained constant for at least 21 dpi, which may enhance the vector capacity of A. aegypti and suggests the presence of a mechanism modulating virus replication in the SG.

【 授权许可】

   
2015 Moura et al.; licensee BioMed Central.

【 图 表 】

Figure 1.

【 参考文献 】

• [1]Gubler DJ: The economic burden of dengue. Am J Trop Med Hyg 2012, 86(5):743-744.
• [2]Murray NE, Quam MB, Wilder-Smith A: Epidemiology of dengue: past, present and future prospects. Clin Epidemiol 2013, 5:299-309.
• [3]Guzman MG, Halstead SB, Artsob H, Buchy P, Farrar J, Gubler DJ, et al.: Dengue: a continuing global threat. Nat Rev Microbiol 2010, 8(Suppl 12):S7-S16.
• [4]Wang E, Ni H, Xu R, Barrett AD, Watowich SJ, Gubler DJ, et al.: Evolutionary relationships of endemic/epidemic and sylvatic dengue viruses. J Virol 2000, 74(7):3227-3234.
• [5]Higa Y: Dengue Vectors and their Spatial Distribution. Trop Med Health 2011, 39(4):17-27.
• [6]Consoli RA, Lourenço-de-Oliveira R: Principais mosquitos de importância sanitária no Brasil. FIOCRUZ, Rio de Janeiro; 1994.
• [7]Gluber D: Dengue and dengue hemorrhagic fever. Clin Microbiol Rev 1998, 11(3):480-496.
• [8]Diallo M, Ba Y, Faye O, Soumare ML, Dia I, Sall AA: Vector competence of Aedes aegypti populations from Senegal for sylvatic and epidemic dengue 2 virus isolated in West Africa. Trans R Soc Trop Med Hyg 2008, 102(5):493-498.
• [9]Rosen L, Roseboom LE, Gubler DJ, Lien JC, Chaniotis BN: Comparative susceptibility of mosquito species and strains to oral and parenteral infection with dengue and Japanese encephalitis viruses. Am J Trop Med Hyg 1985, 34(3):603-615.
• [10]Bennett KE, Olson KE, Munoz M, Fernandez-Salas I, Farfan-Ale JA, Higgs S, et al.: Variation in vector competence for dengue 2 virus among 24 collections of Aedes aegypti from Mexico and the United States. Am J Trop Med Hyg 2002, 67(1):85-92.
• [11]Lambrechts L, Paaijmans KP, Fansiri T, Carrington LB, Kramer LD, Thomas MB, et al.: Impact of daily temperature fluctuations on dengue virus transmission by Aedes aegypti. Proc Natl Acad Sci U S A 2011, 108(18):7460-7465.
• [12]Cox J, Brown HE, Rico-Hesse R: Variation in Vector Competence for Dengue Viruses Does Not Depend on Mosquito Midgut Binding Affinity. PLoS Negl Trop Dis 2011, 5:5. doi:10.1371/journal.pntd.0001172
• [13]Sang R. Dengue in Africa. In: Report of the scientific working group meeting on dengue. Geneva, October 1–5, 2006. WHO Special Programme for Research and Training in Tropical Diseases. 2007. http://www.who.int/tdr/publications/documents/swg_dengue_2.pdf. Accessed Jun 2014.
• [14]Sylla M, Bosio C, Urdaneta-Marquez L, Ndiaye M, Black WC: Gene flow, subspecies composition, and dengue virus-2 susceptibility among Aedes aegypti collections in Senegal. PLoS Negl Trop Dis 2009, 3(4):e408. doi:10.1371/journal.pntd.0000408
• [15]Were F: The dengue situation in Africa. Paediatr Int Child Health 2012, 32(Suppl. 1):18-21.
• [16]Ministério da Saúde de Cabo Verde: Relatório Estatístico 2009. Praia: Gabinete de Estudos, Planeamento e Cooperação do Ministério da Saúde. 2010.
• [17]Franco L, Di Caro A, Carletti F, Vapalahti O, Renaudat C, Zeller H, et al.: Recent expansion of dengue virus serotype 3 in West Africa. Euro Surveill 2010, 15:7.
• [18]Ribeiro H, Cunha Ramos H, Capela RA, Pires CA: Os mosquitos de Cabo Verde, Sistemática, Distribuição, Bioecologia, e Importância Médica. Junta de Investigaçoes Cientifícas do Ultramar, Lisboa; 1980.
• [19]Alves J, Gomes B, Rodrigues R, Silva J, Arez AP, Pinto J, et al.: Mosquito fauna on the Cape Verde Islands (West Africa): an update on species distribution and a new finding. J Vector Ecol 2010, 35(2):307-312.
• [20]Vazeille M, Yebakima A, Lourenco-de-Oliveira R, Andriamahefazafy B, Correira A, Rodrigues JM, et al.: Oral receptivity of Aedes aegypti from Cape Verde for yellow fever, dengue, and chikungunya viruses. Vector Borne Zoonotic Dis 2013, 13(1):37-40.
• [21]Ministério da Agricultura: Alimentação e Ambiente de Cabo Verde. Comunicação Nacional sobre Mudanças Climáticas. Secretariado Executivo para o Ambiente, Praia; 1999.
• [22]Instituto Nacional de Estatística: Censo 2010. INE, Praia; 2010.
• [23]Regis L, Monteiro AM, Melo-Santos MA, SilveiraJr JC, Furtado AF, Acioli RV, et al.: Developing new approaches for detecting and preventing Aedes aegypti population outbreaks: basis for surveillance, alert and control system. Mem Inst Oswaldo Cruz 2008, 103(1):50-59.
• [24]Carvalho-Leandro D, Ayres CF, Guedes DR, Suesdek L, Melo-Santos MA, Oliveira CF, et al.: Immune transcript variations among Aedes aegypti populations with distinct susceptibility to dengue virus serotype 2. Acta Trop 2012, 124(2):113-119.
• [25]Guedes DR: Análise da competência vetorial para o vírus Dengue em populações naturais de Aedes aegypti e Aedes albopictus de Pernambuco. Centro de Pesquisas Aggeu Magalhães, Fundação Oswaldo Cruz, Recife; 2012.
• [26]Xi Z, Ramirez JL, Dimopoulos G: The Aedes aegypti toll pathway controls dengue virus infection. PLoS Pathog 2008, 4(7):e1000098. doi:10.1371/journal.ppat.1000098
• [27]Santos JJ, Cordeiro MT, Bertani GR, Marques ET, Gil LH: Construction and characterisation of a complete reverse genetics system of dengue virus type 3. Mem Inst Oswaldo Cruz 2013, 108(8):983-991.
• [28]Salazar MI, Richardson JH, Sanchez-Vargas I, Olson KE, Beaty BJ: Dengue virus type 2: replication and tropisms in orally infected Aedes aegypti mosquitoes. BMC Microbiol 2007, 7:9. doi:1471-2180-7-9. 10.1186/1471-2180-7-9 BioMed Central Full Text
• [29]Lambrechts L, Chevillon C, Albright RG, Thaisomboonsuk B, Richardson JH, Jarman RG et al. BMC Evol Biol. BMC evolutionary biology. 2009;9:160. doi:1471-2148-9-160. 10.1186/1471-2148-9-160.
• [30]Kong YY, Thay CH, Tin TC, Devi S: Rapid detection, serotyping and quantitation of dengue viruses by TaqMan real-time one-step RT-PCR. J Virol Methods 2006, 138(1–2):123-130.
• [31]Lanciotti RS, Calisher CH, Gubler DJ, Chang GJ, Vorndam AV: Rapid detection and typing of dengue viruses from clinical samples by using reverse transcriptase-polymerase chain reaction. J Clin Microbiol 1992, 30(3):545-551.
• [32]Cordeiro MT: Evolução da dengue no estado de Pernambuco, 1987–2006: Epidemiologia e caracterização molecular dos sorotipos circulantes. Centro de Pesquisas Aggeu Magalhães, Fundação Oswaldo Cruz, Recife; 2008.
• [33]Rico-Hesse R: Microevolution and virulence of dengue viruses. Adv Virus Res 2003, 59:315-341.
• [34]Munoz-Jordan JL, Santiago GA, Margolis H, Stark L: Genetic relatedness of dengue viruses in Key West, Florida, USA, 2009–2010. Emerg Infect Dis 2013, 19(4):652-654.
• [35]Patil JA, Cherian S, Walimbe AM, Patil BR, Sathe PS, Shah PS, et al.: Evolutionary dynamics of the American African genotype of dengue type 1 virus in India (1962–2005). Infect Genet Evol 2011, 11(6):1443-1448.
• [36]Sessions OM, Khan K, Hou Y, Meltzer E, Quam M, Schwartz E, et al.: Exploring the origin and potential for spread of the 2013 dengue outbreak in Luanda, Angola. Glob Health Action 2013, 6:21822. doi:21822.
• [37]Domingo C, Niedrig M, Gascon J, Palacios G, Reyes N, Malo MJ, et al.: Molecular surveillance of circulating dengue genotypes through European travelers. J Travel Med 2011, 18(3):183-190.
• [38]Anderson JR, Rico-Hesse R: Aedes aegypti vectorial capacity is determined by the infecting genotype of dengue virus. Am J Trop Med Hyg 2006, 75(5):886-892.
• [39]Armstrong PM, Rico-Hesse R: Differential susceptibility of Aedes aegypti to infection by the American and Southeast Asian genotypes of dengue type 2 virus. Vector Borne Zoonotic Dis 2001, 1(2):159-168.
• [40]Silva A: Caracterização Molecular dos vírus Dengue circulantes em Pernambuco: implicaçoes epidemiológicas. Centro Pesquisas Aggeu Magalhães, Fundação Oswaldo Cruz, Recife; 2013.
• [41]Gubler DJ, Sather GE, Kuno G, Cabral JR: Dengue 3 virus transmission in Africa. Am J Trop Med Hyg 1986, 35(6):1280-1284.
• [42]Sharp TW, Wallace MR, Hayes CG, Sanchez JL, DeFraites RF, Arthur RR, et al.: Dengue fever in U.S. troops during Operation Restore Hope, Somalia, 1992–1993. Am J Trop Med Hyg 1995, 53(1):89-94.
• [43]Messer WB, Gubler DJ, Harris E, Sivananthan K, De Silva AM: Emergence and global spread of a dengue serotype 3, subtype III virus. Emerg Infect Dis 2003, 9(7):800-809.
• [44]Lanciotti RS, Gubler DJ, Trent DW: Molecular evolution and phylogeny of dengue-4 viruses. J Gen Virol 1997, 78(pt. 9):2279-2284.
• [45]Nunes MR, Faria NR, Vasconcelos HB, Medeiros DB, De Lima CP S, Carvalho VL, et al.: Phylogeography of dengue virus serotype 4, Brazil, 2010–2011. Emerg Infect Dis 2012, 18(11):1858-1864.
• [46]Bosio CF, Beaty BJ, Black WC: Quantitative genetics of vector competence for dengue-2 virus in Aedes aegypti. Am J Trop Med Hyg 1998, 59(6):965-970.
• [47]Tabachnick WJ: Nature, nurture and evolution of intra-species variation in mosquito arbovirus transmission competence. Int J Environ Res Public Health 2013, 10(1):249-277.
• [48]Black WC, Bennett KE, Gorrochotegui-Escalante N, Barillas-Mury CV, Fernandez-Salas I, De Lourdes Munoz M, et al.: Flavivirus susceptibility in Aedes aegypti. Arch Med Res 2002, 33(4):379-388.
• [49]Carrington LB, Seifert SN, Armijos MV, Lambrechts L, Scott TW: Reduction of Aedes aegypti vector competence for dengue virus under large temperature fluctuations. Am J Trop Med Hyg 2013, 88(4):689-697.
• [50]Ramirez JL, Souza-Neto J, Torres Cosme R, Rovira J, Ortiz A, Pascale JM, et al.: Reciprocal tripartite interactions between the Aedes aegypti midgut microbiota, innate immune system and dengue virus influences vector competence. PLoS Negl Trop Dis 2012, 6(3):e1561. doi:10.1371/journal.pntd.0001561 PNTD-D-11-01085.
• [51]Jaenisch T, Junghanss T, Wills B, Brady OJ, Eckerle I, Farlow A, et al.: Dengue expansion in Africa-not recognized or not happening? Emerg Infect Dis 2014, 20:10. doi:10.3201/eid2010.140487
• [52]Guedes DR, Cordeiro MT, Melo-Santos MA, Magalhaes T, Marques E, Regis L, et al.: Patient-based dengue virus surveillance in Aedes aegypti from Recife, Brazil. J Vector Borne Dis 2010, 47(2):67-75.
• [53]Thongrungkiat S, Maneekan P, Wasinpiyamongkol L, Prummongkol S: Prospective field study of transovarial dengue-virus transmission by two different forms of Aedes aegypti in an urban area of Bangkok. Thailand J Vector Ecol 2011, 36(1):147-152.
• [54]Thongrungkiat S, Wasinpiyamongkol L, Maneekan P, Prummongkol S, Samung Y: Natural transovarial dengue virus infection rate in both sexes of dark and pale forms of Aedes aegypti from an urban area of Bangkok, Thailand. Southeast Asian J Trop Med Public Health 2012, 43(5):1146-1152.