1921
Volume 80, Issue 1
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645

Abstract

Concurrent ingestion of microfilariae (mf) and arboviruses by mosquitoes can enhance the transmission of virus compared with when virus is ingested alone. We studied the effect of mf enhancement on the extrinsic incubation period (EIP) of dengue 1 virus within mosquitoes by feeding mosquitoes on blood that either contained virus plus mf or virus only. Mosquitoes were sampled over time to determine viral dissemination rates. Co-ingestion of mf and virus reduced viral EIP by over half. We used the computer simulation program, DENSiM, to compare the predicted patterns of dengue incidence that would result from such a shortened EIP versus the EIP derived from the control (i.e., virus only) group of mosquitoes. Results indicated that, over the 14-year simulation period, mf-induced acceleration of the EIP would generate more frequent (but not necessarily more severe) epidemics. Potential interactions between arboviruses and hematozoans deserve closer scrutiny.

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References

  1. Mellor PS, Boorman J, 1980. Multiplication of bluetongue virus in Culicoides nubeculosus (Meigen) simultaneously infected with the virus and the microfilariae of Onchocerca cervicalis (Railliet & Henry). Ann Trop Med Parasitol 74 : 463–469. [Google Scholar]
  2. Turell MJ, Rossignol PA, Spielman A, Rossi CA, Bailey CL, 1984. Enhanced arboviral transmission by mosquitoes that concurrently ingested microfilariae. Science 225 : 1039–1041. [Google Scholar]
  3. Turell MJ, Mather TN, Spielman A, Bailey CL, 1987. Increased dissemination of dengue 2 virus in Aedes aegypti associated with concurrent ingestion of microfilariae of Brugia malayi. Am J Trop Med Hyg 37 : 197–201. [Google Scholar]
  4. Zytoon EM, El-Belbasi HI, Matsumura T, 1993. Mechanism of increased dissemination of chikungunya virus in Aedes albopictus mosquitoes concurrently ingesting microfilariae of Dirofilaria immitis. Am J Trop Med Hyg 49 : 201–207. [Google Scholar]
  5. Vaughan JA, Turell MJ, 1996. Dual host infections: enhanced infectivity of eastern equine encephalitis virus to Aedes mosquitoes mediated by Brugia microfilariae. Am J Trop Med Hyg 54 : 105–109. [Google Scholar]
  6. Vaughan JA, Trpis M, Turell MJ, 1999. Brugia malayi microfilariae enhance the infectivity of Venezuelan equine encephalitis virus to Aedes mosquitoes. J Med Entomol 36 : 758–763. [Google Scholar]
  7. Chamberlain RW, Sudia WD, 1961. Mechanism of transmission of viruses by mosquitoes. Annu Rev Entomol 6 : 371–390. [Google Scholar]
  8. Kramer LD, Hardy JL, Presser SB, Houk EJ, 1981. Dissemination barriers for western equine encephalomyelitis virus in Culex tarsalis infected after ingestion of low viral doses. Am J Trop Med Hyg 30 : 190–197. [Google Scholar]
  9. Vaughan JA, Bell JA, Turell MJ, Chadee DD, 2007. Passage of ingested Mansonella ozzardi (Spirurida: Onchocercidae) microfilariae through the midgut of Aedes aegypti mosquitoes (Diptera: Culicidae). J Med Entomol 44 : 111–116. [Google Scholar]
  10. Focks DA, Daniels E, Haile DH, Keesling JE, 1995. A simulation model of the epidemiology of urban dengue fever: literature analysis, model development, preliminary validation, and samples of simulation results. Am J Trop Med Hyg 53 : 489–506. [Google Scholar]
  11. Turell MJ, Gargan TP II, Bailey CL, 1984. Replication and dissemination of Rift Valley fever virus in Culex pipiens. Am J Trop Med Hyg 33 : 176–181. [Google Scholar]
  12. Gargan TP, Bailey CL, Higbee GA, Gad A, El Said S, 1983. The effect of laboratory colonization of the vector-pathogen interactions of Egyptian Culex pipiens and Rift Valley fever virus. Am J Trop Med Hyg 32 : 1154–1163. [Google Scholar]
  13. Focks DA, Haile DH, Daniels E, Mount GA, 1993. Dynamic life table model of a container-inhabiting mosquito, Aedes aegypti (L.) (Diptera: Culicidae). Part 1. Analysis of the literature and model development. J Med Entomol 30 : 1003–1017. [Google Scholar]
  14. Focks DA, Haile DH, Daniels E, Mount GA, 1993. Dynamic life table model of a container-inhabiting mosquito, Aedes aegypti (L.) (Diptera: Culicidae). Part 2: Simulation results and validation. J Med Entomol 30 : 1018–1028. [Google Scholar]
  15. Muir LE, Kay BH, 1998. Aedes aegypti survival and dispersal estimated by mark-release-recapture in northern Australia. Am J Trop Med Hyg 58 : 277–282. [Google Scholar]
  16. McLean DM, Clarke AM, Coleman JC, Montalbetti CA, Skidmore AG, Walter TE, Wise R, 1974. Vector capability of Aedes aegypti mosquitoes for California encephalitis and dengue viruses at various temperatures. Can J Microbiol 20 : 255–262. [Google Scholar]
  17. Watts DM, Burke DS, Harrison BA, Whitmire RE, Nisalak A, 1987. Effect of temperature on the vector efficiency of Aedes aegypti for dengue 2 virus. Am J Trop Med Hyg 36 : 143–152. [Google Scholar]
  18. Sharpe PHJ, DeMichele DW, 1977. Reaction kinetics of poikilotherm development. J Theoret Biol 64 : 639–670. [Google Scholar]
  19. Krishnamoorthy K, Subramanian S, Van Oortmarssen GJ, Habbema JD, Das PK, 2004. Vector survival and parasite infection: the effect of Wuchereria bancrofti on its vector Culex quinquefasciatus. Parasit 129 : 43–50. [Google Scholar]
  20. Brito AC, Fontes G, Williams P, Rocha EM, 1998. Bancroftian filariasis in Maceio, state of Alagoas, Brazil: Observations on Culex quinquefasciatus after blood feeding on individuals with different densities of microfilariae in the peripheral blood stream. Am J Trop Med Hyg 58 : 489–494. [Google Scholar]
  21. Russell RC, Geary MJ, 1996. The influence of microfilarial density of dog heartworm Dirofilaria immitis on infection rate and survival of Aedes notoscriptus and Culex annulirostris from Australia. Med Vet Entomol 10 : 29–34. [Google Scholar]
  22. Ibrahim MS, Trpis M, 1987. The effect of Brugia pahangi infection on survival of susceptible and refractory species of the Aedes scutellaris complex. Med Vet Entomol 1 : 329–337. [Google Scholar]
  23. Klowden MJ, 1981. Infection of Aedes aegypti with Brugia pahangi administered by enema: results of quantitative infection and loss of infective larvae during blood feeding. Trans R Soc Trop Med Hyg 75 : 354–358. [Google Scholar]
  24. Melrose W, Rahmah N, 2006. Use of Brugia Rapid dipstick and ICT test to map distribution of lymphatic filariasis in the Democratic Republic of Timor-Leste. Southeast Asian J Trop Med Public Health 37 : 22–25. [Google Scholar]
  25. Supali T, Ismid IS, Wibowo H, Djuardi Y, Majanati E, Ginanjar P, Fischer P, 2006. Estimation of the prevalence of lymphatic filariasis by a pool screen PCR assay using blood spots on filter paper. Trans R Soc Trop Med Hyg 100 : 753–759. [Google Scholar]
  26. Rosen L, 1955. Observations on the epidemiology of human filariasis in French Oceania. Am J Hyg 61 : 219–248. [Google Scholar]
  27. McGreevy PB, Kostrup N, Tao J, McGreevy MM, de Marshall TF, 1982. Ingestion and development of Wuchereria bancrofti in Culex quinquefasciatus, Anopheles gambiae and Aedes aegypti after feeding on humans with varying densities of microfilariae in Tanzania. Trans R Soc Trop Med Hyg 76 : 288–296. [Google Scholar]
  28. Lowichik A, Lowrie RC, 1988. Uptake and development of Wuchereria bancrofti in Aedes aegypti and Haitian Culex quinquefasciatus that were fed on a monkey with low-density microfilaremia. Trop Med Parasit 39 : 227–229. [Google Scholar]
  29. Zielke E, 1992. On the uptake of Wuchereria bancrofti microfilariae in vector mosquitoes of different susceptibility to filarial infection. Angew Parasitol 33 : 91–95. [Google Scholar]
  30. Calheiros ML, Fontes G, Williams P, Rocha EMM, 1998. Experimental infection of Culex (Culex) quinquefasciatus and Aedes (Stegomyia) aegypti with Wuchereria bancrofti. Mem Inst Oswaldo Cruz 93 : 855–860. [Google Scholar]
  31. Samarawickrema WA, Spears GFS, Sone F, Ichimori K, Cummings RF, 1985. Filariasis in Samoa. II. Some factors related to the development of microfilariae in the intermediate host. Ann Trop Med Parasitol 79 : 101–107. [Google Scholar]
  32. Failloux A-B, Raymond M, Ung A, Glaziou P, Martin PMV, Pasteur N, 1994. Variation in the vector competence of Aedes polynesiensis for Wuchereria bancrofti. Parasitol 112 : 19–29. [Google Scholar]
  33. Rahmah N, Ashikin AN, Anuar AK, Ariff RH, Abdullah B, Chan GT, Williams SA, 1998. PCR-ELISA for the detection of Brugia malayi infection using finger-prick blood. Trans R Soc Trop Med Hyg 92 : 404–406. [Google Scholar]
  34. Cox-Singh J, Pomrehn AD, Rahman HA, Zakaria R, Miller AO, Singh B, 1999. Simple blood-spot sampling with nested polymerase chain reaction detection for epidemiology studies on Brugia malayi. Int J Parasitol 29 : 717–721. [Google Scholar]
  35. Supali T, Wibowo H, Ruckert P, Fischer K, Ismid IS, Purnomo, Djuardi Y, Fischer P, 2002. High prevalence of Brugia timori infection in the highlands of Alor Island, Indonesia. Am J Trop Med Hyg 66 : 560–565. [Google Scholar]
  36. Anonymous, 2007. Global programme to eliminate lymphatic filariasis. Wkly Epidemiol Rec 82 : 361–380. [Google Scholar]
  37. Bartlett CM, Anderson RC, 1980. Filarioid nematodes (Filarioidea: Onchocercidae) of Corvus brachyrhynchos brachyrhynchos Brehm in southern Ontario, Canada and a consideration of the epizootiology of avian filariasis. Syst Parasitol 2 : 77–102. [Google Scholar]
  38. Welker GW, 1962. Helminth parasites of the common grackle, Quiscalis quiscula versicolor Veillot in Indiana. PhD dissertation, The Ohio State University, Columbus, OH.
  39. Granath WO, 1980. Fate of the wild avian filarial nematode Chandlerella quiscali (Onchocercidae: Filarioidae) in the domestic chicken. Poult Sci 59 : 996–1000. [Google Scholar]
  40. Stabler RM, 1961. Studies of the age and seasonal variations in the blood and bone marrow parasites of a series of black-billed magpies. J Parasitol 47 : 413–416. [Google Scholar]
  41. Hibler CP, 1963. Onchocercidae (Nematoda: Filarioidea) of the American Magpie, Pica pica hudsonia (Sabine), in northern Colorado. PhD dissertation, Colorado State University, Fort Collins, CO.
  42. Brewer CM, 2006. The potential for microfilarial enhancement of West Nile virus transmission in the Red River Valley of North Dakota and Minnesota to occur. MS thesis, University of North Dakota, Grand Forks, ND.
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  • Received : 19 Jun 2008
  • Accepted : 04 Aug 2008

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