Bulletin de la Société de pathologie exotique

, Volume 104, Issue 4, pp 250–259 | Cite as

Estimation du risque d’introduction du virus de la fièvre de la vallée du Rift en Tunisie par le moustique Culex pipiens

  • G. Krida
  • L. Diancourt
  • A. Bouattour
  • A. Rhim
  • B. Chermiti
  • A. -B. Failloux
Épidémiologie / Epidemiology

Résumé

Le moustique Culex pipiens a été impliqué dans la transmission du virus West Nile en Tunisie. Les caractéristiques bioécologiques de l’espèce ainsi que certains facteurs environnementaux ont favorisé l’émergence de ce virus dans une région jusqu’alors indemne. Ce scénario fait craindre l’émergence d’autres arbovirus dont le virus de la fièvre de la vallée du Rift (FVR) qui affecte principalement les petits ruminants. La proximité de pays où circule le virus de la FVR avec lesquels la Tunisie entretient le commerce d’animaux n’est pas sans risque. Pour mesurer le risque potentiel d’introduction du virus de la FVR en Tunisie, différents aspects ont été étudiés : la compétence vectorielle des populations de Cx. pipiens et leur niveau de différenciation génétique. Nous avons mis en évidence une compétence vectorielle faible vis-à-vis du virus de la FVR et une différenciation forte entre populations témoignant d’une faible capacité de dispersion de l’espèce. Ainsi, nous concluons que même si le virus de la FVR était introduit, l’amplification virale dans le vecteur Cx. pipiens, tout en étant possible, ne serait pas associée à une dissémination du virus par l’intermédiaire du moustique. Toutefois, le caractère émergent du virus de la FVR et la présence d’autres espèces potentiellement vectrices (e.g. Ochlerotatus caspius) doivent imposer le maintien et même le renforcement des surveillances zoosanitaire et entomologique afin de limiter le risque d’introduction et de circulation du virus de la FVR en Tunisie.

Mots clés

Fièvre de la vallée du Rift Culex pipiens Surveillance entomologique Contrôle vétérinaire du bétail Arbovirus Émergence Différenciation génétique Compétence vectorielle Nord-est et centre-est de la Tunisie Maghreb Afrique du Nord 

Assessment of the risk of introduction to Tunisia of the Rift Valley fever virus by the mosquito Culex pipiens

Abstract

The mosquito Culex pipiens has been involved as vector of the West Nile virus in Tunisia. Its bio-ecological characteristics in combination with some environmental factors have favoured the emergence of this virus in a West-Nile free zone. This leads to question about the potential risk of introducing another arbovirus, the Rift Valley fever (RVF) virus, in Tunisia from neighbouring countries where RVF circulates. In this study, we have evaluated the vector competence of different populations of Cx. pipiens towards two strains of RVF virus, the virulent ZH548 and the avirulent Clone 13 by experimental infections and the genetic differentiation of these populations of Cx. pipiens using four microsatellite loci. We found disseminated infection rates ranging from 0% to 14.7% and a high genetic differentiation among populations without any geographical pattern (no isolation by distance). Thus, although Cx. pipiens is able to sustain an amplification of RVF virus, viral dissemination through mosquito dispersal would be unlikely. However, as RVF is an emerging disease transmitted by several other potential mosquito species (e.g. Ochlerotatus caspius), attention should be maintained to survey livestock and mosquitoes in Tunisia.

Keywords

Rift valley fever Arbovirus Culex pipiens Entomologic surveillance Veterinary control of cattle Emergence Genetic differentiation Vector competence North-east and centre-east Tunisia Maghreb Northern Africa 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Références

  1. 1.
    Apperson CS, Harrison BA, Unnasch TR, et al (2002) Host-feeding habits of Culex and other mosquitoes (Diptera: Culicidae) in the borough of Queens in New York City, with characters and techniques for identification of Culex mosquitoes. J Med Entomol 39(5):777–785PubMedCrossRefGoogle Scholar
  2. 2.
    Arthur RR, El Sharkawy MS, Cope SE, et al (1993) Recurrence of Rift Valley Fever in Egypt. Lancet 342(8880):1149–1150PubMedCrossRefGoogle Scholar
  3. 3.
    Brownie J, Shawcross S, Theaker J, et al (1997) The elimination of primer-dimer accumulation in PCR. Nucleic Acids Res 25(16):3235–3241PubMedCrossRefGoogle Scholar
  4. 4.
    Brunhes J, Rhaiem A, Geoffroy B, Hervy JP (2000) Les moustiques de l’Afrique méditerranéenne. Logiciel d’identification et d’enseignement. IRD et IPT, CD-ROM Collection didactique IRD Éditions, Montpellier, FranceGoogle Scholar
  5. 5.
    Byrne K, Nichols R (1999) Culex pipiens in London underground tunnels: differentiation between surface and subterranean populations. Heredity 82(Pt1):7–15PubMedCrossRefGoogle Scholar
  6. 6.
    Dahl C (1988) Taxonomic studies on Culex pipiens and Cx. torrentium. Biosystematics of Haematophagous insects. Oxford Systematics Association, Oxford, pp 149–175Google Scholar
  7. 7.
    Dancesco P, Chadli A, Kchouk M, Horac M (1975) À propos d’un biotope saisonnier hivernal autogenicus. Bull Soc Pathol Exot Filiales 68(5):503–508PubMedGoogle Scholar
  8. 8.
    Daubney R, Hudson JR, Garnham PC (1931) Enzootic hepatitis or Rift Valley Fever: an undescribed virus disease of sheep, cattle and man from East Africa. J Pathol Bacteriol 34:545–549CrossRefGoogle Scholar
  9. 9.
    Dobzhansky T (1937) Genetics and the Origin of Species. In: The Columbia classics in evolutionary series. Columbia Univ. Press, New York, 364 pGoogle Scholar
  10. 10.
    Dobzhansky T, Pavan C (1943) Studies on Brazilian species of Drosophila. Bolm Fac Filos Cienc S Paulo 36: 7–72Google Scholar
  11. 11.
    Durand JP, Simon F, Tolou H (2004) Virus West Nile: à nouveau en France chez l’homme et les chevaux. Rev Prat 54(7):703–710PubMedGoogle Scholar
  12. 12.
    El Harrak M, Le Guenno B, Gounon P (1997) Isolement du virus West Nile au Maroc. Virologie 1:248–249Google Scholar
  13. 13.
    Faraj C, Elkohli M, Lyagoubi M (2006) Cycle gonotrophique de Culex pipiens (Diptera: Culicidae), vecteur potentiel du virus West Nile, au Maroc: estimation de la durée en laboratoire. Bull Soc Pathol Exot 99(2):119–121 [http://www.pathexo.fr/documents/articles-bull/T99-2-2846-3p.pdf]PubMedGoogle Scholar
  14. 14.
    Farid HA, Hammad RE, Hassan MM, et al (2001) Detection of Wuchereria bancrofti in mosquitoes by the polymerase chain reaction: a potentially useful tool for large-scale control programmes. Trans R Soc Trop Med Hyg 95(1):29–32PubMedCrossRefGoogle Scholar
  15. 15.
    Fonseca DM, Keyghobadi N, Malcolm CA, et al (2004) Emerging vectors in the Culex pipiens complex. Science 303(5663):1535–1538PubMedCrossRefGoogle Scholar
  16. 16.
    Fonseca DM, LaPointe DA, Fleischer RC (2000) Bottlenecks and multiple introductions: population genetics of the vector of avian malaria in Hawaii. Mol Ecol 9(11):1803–1814PubMedCrossRefGoogle Scholar
  17. 17.
    Garbouj M, Bejaoui M, Aloui H, Ben Ghorbal M (2003) La maladie du Nil occidental. Bull Epidemiol 3:4–6Google Scholar
  18. 18.
    Gerrard SR, Bird BH, Albariño CG, Nichol ST (2007) The NSm proteins of Rift Valley fever virus are dispensable for maturation, replication and infection. Virology 359(2):459–465. (Epub 2006 Oct 30)PubMedCrossRefGoogle Scholar
  19. 19.
    Giorgi C, Accardi L, Nicoletti L, et al (1991) Sequences and coding strategies of the S RNAs of Toscana and Rift Valley fever viruses compared to those of Punta Toro, Sicilian Sandfly fever, and Uukuniemi viruses. Virology 180(2):738–753PubMedCrossRefGoogle Scholar
  20. 20.
    Gomes B, Sousa CA, Novo MT, et al (2009) Asymmetric introgression between sympatric molestus and pipiens forms of Culex pipiens (Diptera: Culicidae) in the Comporta region, Portugal. BMC Evol Biol 9:262PubMedCrossRefGoogle Scholar
  21. 21.
    Gubler DJ, Nalim S, Tan R, et al (1979) Variation in susceptibility to oral infection with dengue viruses among geographic strains of Aedes aegypti. Am J Trop Med Hyg 28(6):1045–1052PubMedGoogle Scholar
  22. 22.
    Harbach RE, Harrison BA, Gad AM (1984) Culex molestus Forskål (Diptera: Culicidae): neotype designation, description, variation and taxonomic status. Proc Entomol Soc Wash 86:521–542Google Scholar
  23. 23.
    Hamer GL, Walker ED, Brawn JD, et al (2008) Rapid amplification of West Nile virus: the role of hatch-year birds. Vector Borne Zoonotic Dis 8(1):57–67PubMedCrossRefGoogle Scholar
  24. 24.
    Hayes CG (2001) West Nile virus: Uganda, 1937, to New York City, 1999. Ann N Y Acad Sci 951:25–37PubMedCrossRefGoogle Scholar
  25. 25.
    Hoogstraal H, Meegan JM, Khalil GM, Adham FK (1979) The Rift Valley fever epizootic in Egypt 1977–1978. 2. Ecological and entomological studies. Trans R Soc Trop Med Hyg 73(6):624–629PubMedCrossRefGoogle Scholar
  26. 26.
    Huang S, Hamer GL, Molaei G, et al (2009) Genetic variation associated with mammalian feeding in Culex pipiens from a West Nile virus epidemic region in Chicago, Illinois. Vector Borne Zoonotic Dis 9(6):637–642PubMedCrossRefGoogle Scholar
  27. 27.
    Hubby JL, Lewontin RC (1966) A molecular approach to the study of genic heterozygosity in natural populations. I. The number of alleles at different loci in Drosophila pseudoobscura. Genetics 54(2):577–594PubMedGoogle Scholar
  28. 28.
    Juminer B, Kchouk M, Rioux JA, Ben Osman F (1964) À propos des culicidés vulnérants de la banlieue littorale de Tunis. Arch Inst Pasteur Tunis 41(2):23–32Google Scholar
  29. 29.
    Jup PG, Kemp A, Grobbelaar A, et al (2002) The 2000 epidemic of Rift Valley fever in Saudi Arabia: mosquito vector studies. Med Vet Entomol 16(3):245–252PubMedCrossRefGoogle Scholar
  30. 30.
    Keyghobadi N, Matrone M, Ebel GD, et al (2004) Microsatellite loci from the northern house mosquito (Culex pipiens), a principal vector of West Nile virus in North America. Mol Ecol Notes 4:20–22CrossRefGoogle Scholar
  31. 31.
    Kilpatrick AM, Daszak P, Jones MJ, et al (2006) Host heterogeneity dominates West Nile virus transmission. Proc Biol Sci 273(1599):2327–2333PubMedCrossRefGoogle Scholar
  32. 32.
    Kilpatrick AM, Kramer LD, Jones MJ, et al (2007) Genetic influences on mosquito feeding behavior and the emergence of zoonotic pathogens. Am J Trop Med Hyg 77(4):667–671PubMedGoogle Scholar
  33. 33.
    Krida G, Rhaiem A, Bouattour A (1997) Effet de la qualité des eaux sur l’expression du potentiel biotique du moustique Culex pipiens L. dans la région de Ben Arous (sud de Tunis). Bull Soc Entomol France 102(2):143–150Google Scholar
  34. 34.
    Kuberski TT, Rosen L (1977) A simple technique for the detection of dengue antigen in mosquitoes by immunofluorescence. Am J Trop Med Hyg 26(3):533–537PubMedGoogle Scholar
  35. 35.
    Laven H (1951) Crossing experiments with Culex strains. Evolution 5:310–375CrossRefGoogle Scholar
  36. 36.
    Le Guenno B, Bougermouh A, Azzam T, Bouakaz R (1996) West Nile: a deadly virus? Lancet 348(9037):1315PubMedCrossRefGoogle Scholar
  37. 37.
    Lee DS, Yoon HK, Kim HS, Lee KW (1970) Studies on the life cycle of Culex pipiens pallens in Korea. Kisaengchunghak Chapchi 8(1):36–38PubMedGoogle Scholar
  38. 38.
    Lewontin RC, Hubby JL (1966) A molecular approach to the study of genic heterozygosity in natural populations. II. Amount of variation and degree of heterozygosity in natural populations of Drosophila pseudoobscura. Genetics 54(2):595–609PubMedGoogle Scholar
  39. 39.
    Linthicum KJ, Bailey CL, Davies FG, Tucker CJ (1987) Detection of Rift Valley fever viral activity in Kenya by satellite remote sensing imagery. Science 235(4796):1656–1659PubMedCrossRefGoogle Scholar
  40. 40.
    Linthicum KJ, Davies FG, Kairo A, Bailey CL (1985) Rift Valley fever virus (family Bunyaviridae, genus Phlebovirus). Isolations from Diptera collected during an inter-epizootic period in Kenya. J Hyg (Lond) 95(1):197–209CrossRefGoogle Scholar
  41. 41.
    Mattingly PF, Rozeboom LE, Knight KL, et al (1951) The Culex pipiens complex. Trans Roy Ent Soc London 102:331–382CrossRefGoogle Scholar
  42. 42.
    Mayr E (1942) Systematics and the Origin of Species. Columbia University Press, New YorkGoogle Scholar
  43. 43.
    Meegan JM (1979) The Rift Valley fever epizootic in Egypt 1977–1978. 1. Description of the epizzotic and virological studies. Trans R Soc Trop Med Hyg 73(6):618–623PubMedCrossRefGoogle Scholar
  44. 44.
    Meegan JM, Bailey CL (1988) Rift Valley fever. In: Monath TP (ed) The arboviruses: epidemiology and ecology. CRC Press, Boca Raton, FL, pp 61–76Google Scholar
  45. 45.
    Meegan JM, Khalil GM, Hoogstraal H, Adham FK (1980) Experimental transmission and field isolation studies implicating Culex pipiens as a vector of Rift Valley fever virus in Egypt. Am J Trop Med Hyg 29(6):1405–1410PubMedGoogle Scholar
  46. 46.
    Morvan J, Rollin PE, Laventure S, et al (1992) Rift Valley fever epizootic in the central highlands of Madagascar. Res Virol 143(6):407–415PubMedCrossRefGoogle Scholar
  47. 47.
    Moutailler S, Bouloy M, Failloux AB (2007) Short report: efficient oral infection of Culex pipiens quinquefasciatus by Rift Valley fever virus using a cotton stick support. Am J Trop Med Hyg 76(5):827–829PubMedGoogle Scholar
  48. 48.
    Moutailler S, Krida G, Schaffner F, et al (2008) Potential vectors of Rift Valley Fever virus in the Mediterranean Region. Vector Borne Zoonotic Dis 8(6):749–753PubMedCrossRefGoogle Scholar
  49. 49.
    Murgue B, Murri S, Zientara S, et al (2001) West Nile outbreak in horses in southern France, 2000: the return after 35 years. Emerg Infect Dis 7(4):692–696PubMedCrossRefGoogle Scholar
  50. 50.
    Nabeth P, Kane Y, Abdalahi MO, et al (2001) Rift Valley fever outbreak, Mauritania, 1998: seroepidemiologic, virologic, entomologic, and zoologic investigations. Emerg Infect Dis 7(6):1052–1054PubMedCrossRefGoogle Scholar
  51. 51.
    Nudelman S, Galun R, Kitron U, Spielman A (1988) Physiological characteristics of Culex pipiens populations in the middle East. Med Vet Entomol 2(2):161–169PubMedCrossRefGoogle Scholar
  52. 52.
    OMS (2007) Fièvre de la vallée du Rift dans l’Union des Comores. Bull Hebdo Int no 1036Google Scholar
  53. 53.
    OMS (2008) Fièvre de la Vallée du Rift au Soudan. Bull Epidemiol Hebdo no5Google Scholar
  54. 54.
    Richards AG (1941) Differentiation between toxic and suffocating effects of petroleum oils on larvae of the house mosquito (Culex pipiens L.) [Diptera]. Trans Am Entomol Soc 67:161–196Google Scholar
  55. 55.
    Rioux JA, Juminer B, Kchouk M, Croset H (1965) Présence du caractère autogène chez Culex piplens pipiens L. dans un biotope épigé de l’Île de Djerba. Arch Inst Pasteur Tunis 42:1–8Google Scholar
  56. 56.
    Roubaud E (1933) Essai synthétique sur la vie du moustique commun Culex pipiens (L.). Ann Sc Nat Bot Zool 16: 165–168Google Scholar
  57. 57.
    Roubaud E (1939) Le pouvoir autogène chez le biotype nordafricain du moustique commun Culex pipiens (L.). Bull Soc Pathol Exot 32:172–175Google Scholar
  58. 58.
    Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145(4):1219–1228PubMedGoogle Scholar
  59. 59.
    Smith JL, Fonseca DM (2004) Rapid assays for identification of members of the Culex (Culex) pipiens complex, their hybrids, and other sibling species (Diptera: Culicidae). Am J Trop Med Hyg 70(4):339–345PubMedGoogle Scholar
  60. 60.
    Spielman A (2001) Structure and seasonality of Nearctic Culex pipiens populations. Ann NY Acad Sci 951:220–234PubMedCrossRefGoogle Scholar
  61. 61.
    Subra R (1982) The distribution and frequency of Culex pipiens quinquefasciatus Say 1823 (Diptera, Culicidae) breeding places on the Kenya Coast in relation to human sociological factors. J Trop Med Hyg 85(2):57–61PubMedGoogle Scholar
  62. 62.
    Tempelis CH (1975) Host-feeding patterns of mosquitoes, with a review of advances in analysis of blood meals by serology. J Med Entomol 11(6):635–653PubMedGoogle Scholar
  63. 63.
    Tesh RB, Gubler DJ, Rosen L (1976) Variation among geographic strains of Aedes albopictus in susceptibility to infection with chikungunya virus. Am J Trop Med Hyg 25(2):326–335PubMedGoogle Scholar
  64. 64.
    Triki H, Murri S, Le Guenno B, et al (2001) Méningoencéphalite à arbovirus West Nile en Tunisie. Med Trop 61(6):487–490Google Scholar
  65. 65.
    Tsai TF, Mitchell CJ (1989) St Louis encephalitis. In: Monath TP (ed) The arboviruses: epidemiology and ecology. CRC Press, Boca Raton, FL, pp 113–143Google Scholar
  66. 66.
    Turell MJ, O’Guinn ML, Dohm DJ, Jones JW (2001) Vector competence of North American mosquitoes (Diptera: Culicidae) for West Nile virus. J Med Entomol 38(2):130–134PubMedCrossRefGoogle Scholar
  67. 67.
    Vermeil C (1954) Nouvelle contribution à l’étude du complexe Culex pipiens en Tunisie. Bull Soc Pathol Exot 47:841–843Google Scholar
  68. 68.
    Villani F, Urbanelli S, Gad A, et al (1986) Electrophoretic research on populations of Egyptian and Israeli Culex pipiens (Diptera, Culicidae). Ann Ist Super Sanita 22(1):373–375PubMedGoogle Scholar
  69. 69.
    Vinogradova EB (2000) Mosquitoes Culex pipiens pipiens: taxonomy, distribution, ecology, physiology, genetics, applied importance and control. Pensoft Pulishers, Sofia, 280 pGoogle Scholar
  70. 70.
    Walsh J (1988) Rift Valley fever rears its head. Science 240(4858):1397–1399PubMedCrossRefGoogle Scholar
  71. 71.
    Woods CW, Karpati AM, Grein T, et al (2002) An outbreak of Rift Valley Fever in Northeastern Kenya, 1997–1998. Emerg Infect Dis 8(2):138–144PubMedCrossRefGoogle Scholar
  72. 72.
    Wright S (1931) Evolution in Mendelian populations. Genetics 16(2):97–159PubMedGoogle Scholar
  73. 73.
    Zeller HG, Fontenille D, Traore-Lamizana M (1997) Enzootic activity of Rift Valley fever virus in Senegal. Am J Trop Med Hyg 56(3):265–272PubMedGoogle Scholar
  74. 74.
    Zimmerman JH, Hanafi HA, Abbassy MM (1985) Host-feeding patterns of Culex mosquitoes (Diptera: Culicidae) on farms in Gharbiya Governorate, Egypt. J Med Entomol 22(1):82–87PubMedGoogle Scholar

Copyright information

© Springer Verlag France 2010

Authors and Affiliations

  • G. Krida
    • 1
    • 2
  • L. Diancourt
    • 3
  • A. Bouattour
    • 1
  • A. Rhim
    • 1
  • B. Chermiti
    • 4
  • A. -B. Failloux
    • 5
  1. 1.Institut Pasteur de Tunisservice d’entomologie médicaleTunis BelvédèreTunisie
  2. 2.Institut national agronomique de TunisieTunis MahrajèneTunisie
  3. 3.Institut Pasteur, plateforme génotypage des pathogènes et santé publiqueParis cedex 15France
  4. 4.Institut supérieur agronomique de Chott-MariemChott Mériem, SousseTunisie
  5. 5.Institut Pasteurunité de génétique moléculaire des BunyavirusParis cedex 15France

Personalised recommendations