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Vertical Transmission of Dengue 1 Virus By 118 JouRNer,oF THE Arr,rpnrclNMosqurro CourRor, Assocrertorl VoL.7,No. 1 VERTICAL TRANSMISSIONOF DENGUE 1 VIRUS BY HAEMAGOGUSEQUINUS MOSQUITOES MARK os SOUZA AND JEROME E. FREIERI YaleArbouirus ResearchUnit, Departm.entof Epidemiologyand Public Health, Yale (JniuersityMedical School, 60 CollegeStreet, New Hauen, CT 06501 ABSTRACT' Vertical transmissionof deleue type 1 virus was demonstratedby a st rain of Haemagogus equinus mosquitoesfrom Panama. Parental femaleswere infected by intrathoracic inoculation ,"i 699 production was stimulated by feeding on mice. Dengue 1 virus wis detected in fourth instar larvlj progeny obtained from two installment hatches of eggs.Minimum filial infection rates ranged up to 1:495. The cyclic nature of dengue virus epidemics colonizedin 1980,were used to assayF1 progeny and how these viruses are maintained in areas from vertical transmissionexperiments. where epidemicshave occurred previously pose Mosquitoes were reared at a temperature of unresolved questions. Hereditary passage of 28'Cand aRHof 85%withaphotoperiodof 16 dengueviruses in vector mosquitoesis a possible h light and 8 h dark. Installment hatching was mechanismfor the natural maintenanceof these used to obtain larvae from I1g. equinus eggs. viruses. Laboratory studies have demonstrated This entailed drying eggsfor 1 wk, flooding eggs, vertical passageof all 4 dengue serotypes by drying them again for 1 wk, and then reflooding. females of Aedesalbopictus (Skuse), Ae. aegypti This cyclewas repeated2-3 times. Larvae were (Linn.) (Rosenet al. 1983),by 8 speciesof the fed a suspensionof rabbit chow and adults were Ae. scutellarlsgroup (Freier and Rosen 1987) givenl0%osucrose as a carbohydratesource. and by Ae. mediouittatus(Coq.) (Freier and Ro- A dengue type 1 virus strain, originally iso- sen 1988).Field isolations of dengrrevirus have lated in 1975 from human serum in Suva, Fiji, recoveredtype 2 virus from Ae. aegypti larvae in was used in all experiments. The strain had Burma (Khin and Than 1983) and type 4 virus undergone 3 mosquito passagesin Toxorhyn- from larvae of the same species in Trinidad chites amboinensls (Doleschall) and had never (Hull et al. 1984).Dengue type 2 virus was also been passed in either mice or tissue culture. isolatedin Africa from a pool containinga mix- Stockpools of virus werestored in l-ml aliquots ture of Ae. furcifer (Edwards) and Ae. taylori at -70'C. Edwardsmale mosquitoes(Cornet et al. 1984). Cage-mated Hg. equinus female mosquitoes These field observations further support the wereinoculated intrathoracically with 0.L7pl of contention that vertical transmission may be a denguetype 1 virus about 5-7 days after emer- natural survival mechanismfor dengueviruses. gence.Inoculated mosquitoeswere held at 28'C The goal of our experimentswas to determine for 7 days. On the 7th day after infection, and 1 if denguetype 1 virus could be transmitted ver- wk thereafter, female mosquitoeswere provided tically by the sylvan mosquito, Haemagogus with an uninfected mouse as a blood source to equinus Theobald. This forest canopy species stimulate egg production. Infection of parental from Central and South America also breeds in female Hg. equinus was confirmed by head man-madecontainers, inhabits peridomestic en- squashassay 14 or more days after inoculation. vironments and is attracted to human hosts. Eggs were collected en rnosseon moistened Haemagogtrsequinus has also been incriminated strips of dark brown blotter paper.After removal as a vector of yellow fever (YF) virus (Trapido from oviposition jars, ovistrips were stored at and Galindo1956), and vertical transmissionof 28"C in 85% RH for 1 wk. Installment hatching YF virus by this specieswas demonstrated by was carried out at weekly intervals. Two or 3 Dutary and LeDuc (1981). floodings were performed for each F1 eggcollec- A strain of Hg. equinus from Panama, colo- tion. Larvae from each installment were main- nized in 1975, was used in our tests. Aedes tained separately.Immature stageswere divided aegypti mosquitoesfrom Villalba, Puerto Rico, into pools of 50 fourth instar larvae or pupae and triturated in a Ten Broeck tissue grinder with 1.0-ml phosphate-bufferedsaline (pH 7.a) IPresent gelatin, address: Division of Vector-Borne Infec- containing 0.57o 30% heat-inactivated tious Diseases,Center for Infectious Diseases,Centers fetal calf serum(56"C for 30 min) and antibiotics for Disease Control, Public Health Service, U.S. De- (200 units/ml penicillin and 200 /rg/ml strepto- partment of Health and Human Service, P.O. Box mycin). Larval suspensionswere clarified by 2087. Fort Collins. CO 80522. centrifugationat 1,000x g for 30 min at 4"C. MARCH 1991 OPERATIONAL AND SCIENTIFIC NOTES Each undiluted supernatant suspension was obtained for vertical transmission of YF virus then tested for the presenceof virus by inocu- in parenterally infected females of the same Iating 0.17 pl into 10-15 male or female Ae. strain of Hg. equinus PANAMA that we used aegypti.Assay mosquitoeswere held for 14 days (Dutary and LeDuc 1981). at 28"C. Infected larvae were obtained after the second Mosquitoes were tested for the presence of egg immersion.Recovery of virus from install- dengue type 1 virus by the head squash tech- ment-hatched eggs is an important factor for nique (Kuberski and Rosen1977). The indirect virus maintenance. This finding was also ob- fluorescent antibody test was used with anti- servedby Beaty et al. (1980)with the AMPHUR denguetype 1 mousehyperimmune ascitic fluid strain of Ae. aegypti infected by intrathoracic and fluorescein isothiocyanate-conjugatedanti- inoculationwith YF virus.Vertical transmission mouse goat serum. Specimenswere examined combined with installment hatching is more with a Leitz transmission fluorescent micro- Iikely to ensure Ionger survival of a virus. scope at 200x magnification. At least 3 speci- Although our data are preliminary, the poten- menswere viewed before a pool was considered tial for Hg. equinus, and possibly other sylvatic negative.A pool was consideredpositive when mosquito species that have drought-resistant fluorescencewas observedfor at least one of 5 eggs,to become maintenance hosts for dengue specimensexamined. virusesmust be considered.These species might Vertical transmissionof denguevirus was ob- serve as reservoirs for the survival of dengue servedfor the Panamanianstrain of Hg. equinus viruses during periods of adverseclimatic con- (Table 1). Of the 2,656 F1 larvae and pupae ditions or when susceptiblevertebrates are few tested for the presenceof virus, 4 of 92 pools in number. Vertical transmission would enhance contained dengue type 1 virus. Virus was re- such a possibility by allowing virus persistence covered in our second experiment in which during unusually dry periods. In addition, the larger numbers of progeny were available for peridomestic behavior of Hg. equimzs(Chadee testing. In experiment 2, dengue type 1 virus et al. 1981)might permit this speciesto act as a was recovered from F1 progeny obtained from vector of dengue virus in rural communities both first and second egg installment hatches. located near forests. One could also hypothesize The minimum filial infection rate (MFIR) was that a sylvatic cycle of dengue virus activity 1:495 for the first hatching and 1:750 for the involving Hg. equinus and other Haem.agogus second;the overall MFIR was 1:664.Also, in speciesmight be perpetuatedthrough horizontal experiment2,22 pools of 1,055pupae derived transmission among monkeys present in the from the second egg hatch were assayed for forest canopy. Such a zoonotic system of viral dengr.revirus and all were negative.Examination maintenance was proposed for Southeast Asia of parental femalemosquitoes held 14 days after by Rudnick (1978).Haernagogus equinus feeding inoculation showed that all were infected with on cebusmonkeys and marmosetshas been re- dengue1 virus. ported by Waddell and Taylor (1945,1947), and The frequencyof vertical transmission for Hg. Hg. capricornii Lutz was found by Bugher et al. equinus (l:622) in our study was higher than (1944)to be responsiblefor YF virus transmis- that reported by Rosen et al. (1983) for Ae. sion among marsupials and monkeys in a for- aegyptiVILLALBA (1:1,543)but Iessthan that ested region of eastern Colombia.New World reported by them for Ae. albopictus(1:200). monkeys, such as Alouatta and Cebus,are re- Their experimentswere conductedwith parental ported to be susceptibleto infection with dengue femalesinfected with the same strain of dengue virus as determined by virus isolation and anti- tlpe 1 virus used in our study. Although not body production (Rosen1958). directly comparable,the MFIR results obtained The authors thank Robert E. Shopeand Rob- in our study werehigher than the 1:1,727MFIR ert B. Tesh for providing facilities. We also Table 1. Minirnum filial infection rates (MFIR) fot Hoernagogus equinus F1 progeny obtained from the first ovarian cycle offemales infected parenterally with dengue type 1 virus. No. pools pos/ Exp. no. Egg hatch No. progeny total MFIR lst 0 2nd T52L,P" olL 3rd 15L 0/1 1st 989 L, P 2/2r l:495 2nd 1500L, P 2/30 1:750 .L:larvae;P:pupae. JouRNar oF THE AvnRrcen Moseutro CoNrRol AssocretroN VoL.7, No. I thank Thomas H. G. Aitken and D. Bruce 1984.Natural transovarial transmission of dengr-re Francy for helpful commentson the manuscript. 4 virus in Aedes aegypti in Trinidad. Am. J. Trop. This work was supported in part by NIH grant Med. Hyg. 33:1248.125O. AI 17995to Leon Rosen. Khin, M. M. and K. A. Than. 1983. Transovarial transmission of dengue2 virus by Aedes aegypti in REFERENCESCITED nature.Am. J. Trop. Med. Hyg. 32:590-594. Kuberski, T. T. and L. Rosen. 1977.A simple tech- Beaty,B. J., R. B. Teshand T. H. G. Aitken.1980. nique for the detection of antigen in mosquitoesby Transovarial transmission of yellow fever virus in immunofluorescence.Am. J. Trop. Med. Hyg. Stegomyia mosquitoes. Am. J. Trop. Med. Hyg. 26:533-537. 29:1.25132. Rosen,L. 1958.Experimental infection of New World Bugher,J. C., J. Boshell-Manrique,M.
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