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Vector Competence of Three North American Strains of Aedes Albopiczus for West Nile Virus'

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Vector Competence of Three North American Strains of Aedes Albopiczus for West Nile Virus' Journal of the American Mosquito Control Association, l81@):ZB4-2g9.2OO2 Copyright @ 2002 by the American Mosquito Control Association, Inc. VECTOR COMPETENCE OF THREE NORTH AMERICAN STRAINS OF AEDES ALBOPICZUS FOR WEST NILE VIRUS' MICHAEL R. SARDELIS,',3 MICHAEL J. TURELL,{5 MONICA L. O'GUINN,4 RICHARD G. ANDRE'ENO DONALD R. ROBERTS' ABSTRACT To evaluate the potential for North American (NA) Aezle.salbopictus to transmit West Nile virus (WN)' mosquito strains derived from 3 NA sources (Frederick County, Marylind, FRED strain; Cheverly, MD, CHEV strain; Chambers and Liberty counties, Texas, TAMU strain) were tested. These strains were tested along with a previously tested strain from a Hawaiian source (OAHU strain). Mosquitoes were fed on 2- to 3-day-old chickens previously inoculated with a New York strain (Crow 397-99) of WN. All of the NA strains were competent laboratory vectors of WN, with transmission rates of 36, 50, 83, and 92Vo for the FRED, CHEy OAHU' and TAMU strains, respectively. The extrinsic incubation period for WN in Ae. albopictus held at 26"C was estimated to be lo days. Based on efficiency of viral transmission, evidence of natural infection, bionomics, and distribution, Ae. albopictzs could be an important bridge vector of WN in the southeastern USA. KEY WORDS Aedes albopictus, West Nile virus, vector competence, extrinsic incubation INTRODUCTION Since discovery of Ae. albopictus in Memphis, TN (Reiter and Darsie 1984), and Houston. TX West Nile virus (WN) was reported for the lst (Sprenger and Wuithiranyagool 1986), in the 1980s, time in the Western Hemisphere in 1999 and caused this species has become established throughout encephalitis in humans in New york City and an most of the southeastern USA, extending epizootic in native and exotic avian populations as far north as New Jersey (Moore and Mitchell 1997). (Centers for Disease Control and prevention ICDCI Throughout its range in the USA, Ae. albopictus is 1999a, 1999b; Lancioui et al. 2000). Testing field- an important human pest, aggressively biting dur- collected mosquitoes for evidence of WN infection ing daylight hours close to its breeding sites. Ex- during 1999 and 2000 indicated that Culex pipiens perimental transmission studies indicate that it is a L. is the primary vector of this virus and that a competent vector of several flaviviruses (Mitchell number of additional species may be secondary or 1991). Although it is relarively refractory to infec- bridge vectors (CDC 1999b,2000). potential sec- tion with St. Louis encephalitis virus (Savage et al. ondary or bridge vector species from which mul- 1994), a study with a strain of WN from the our- tiple instances of WN infection were reported in- break of WN in New York in 1999 indicated that clude Culex restuans Theobald, Culex salinarius Ae. albopictus is a highly efficient laboratory vector Coquillett, Aedes vexans (Meigan), Ochlerotatus of WN (Turell et al. 2001). However. the latter japonicus japonicus (Theobald), Ochlerotatus tris- study used a long-colonized strain of Ae. eriatus (Say), Ochlerotatus trivittatzs (Coquillett), albopictus from Hawaii, and therefore may not represent what and Culiseta melanura (Coquillett). In September occurs in nature in regions of the USA where 2000, a single pool of Aedes albopictus (Skuse) WN is now enzootic. collected in southeastern Pennsylvania showed ev- To elucidate the potential role of Ae. idence of WN infection (CDC 2000). albopictus in the epidemiology of WN in the eastern USA, we conducted laboratory studies of the vector compe- I tence of 4 strains: The views of the authors do not necessarily reflect the 2 newly colonized ones from position of the Department of Defense or the Department Maryland where WN is considered enzootic, a of the Army. In conducting research with animals, the long-colonized Texan strain, and the Hawaiian investigators adhered to the Guide for the care and use of strain (OAHU) used by Turell et al. (2001). Addi- laboratory animals, as prepared by the Committee on tionally, studies were done to evaluate viral repli- Care and Use of Laboratory Animals of the Institute of cation and dissemination in these mosquitoes over Laboratory Animal Resources, National Research Council time. (NIH Publication 86-23, Revised 1996). The facilities are fully accredited by the Association for Assessment and Accreditation of Laboratory Animal Care, International. 2 MATERIALS AND METHODS Division of Tropical Public Health, Department of pre- ventive Medicine and Biometrics, Uniformed Services Mosquitoes: Three North American (NA) strains University of the Health Sciences, 4301 Jones Bridge of Ae. albopictus were evaluated for their ability Road, Bethesda. MD 20814. to I transmit WN. These included the Frederick (FRED) Present address: U.S. Army Medical Research Unit- Kenya, Unit 64109, APO AE 09831-4t09. strain, derived from eggs collected in Frederick 4 Department of Vector Assessment, Virotogy Divisron, County, Maryland, in July 1999 (Sardelis and Tur- U.S. Army Medical Research Institute of Infectious Dis- ell 20Ol); the Cheverly (CHEV) strain, derived eases, 1425 Porter Street, Frederick, MD 21702-5011_ from larvae collected from discarded tires in Chev- 5 To whom correspondence should be addressed. erly, Prince George's County, Maryland, in June 284 DucrNleen2002 Vecror. CoMpETENcEop Arots tnoptcrus 285 1999; and the Texas A&M University (TAMU) evaluate viral replication and dissemination over strain, derived from specimens collected in Cham- time, each strain of mosquito was fed on a single bers and Liberty counties, Texas, in 1987. Addi- chicken that had been inoculated with WN 48 h tionally, the OAHU strain of Ae. albopictus, de- earlier. Immediately after ingesting the infectious rived from specimens collected in Honolulu, HI, in blood meal, 5 mosquitoes of each strain were 1971, was evaluated. The generation tested was F3 killed, triturated, frozen, and assayed as described for FRED and CHEY and )F.o for TAMU and above. Handling and maintenance after bloodfeed- -+ OAHU. Larvae were reared at 26 l'C and a 16- ing for the remaining mosquitoes was as described h photoperiod and fed ground catfish chow above, except that samples of 10 mosquitoes of (AquaMax Pond Plus 3000, Purina Mills, Inc., St. each strain were killed, ground, and frozen for later Louis, MO). assay on days 1, 4,7, lO, 14,21, and 28 after Virus and virus assay: The WN strain (Crow bloodfeeding. 397-99) was isolated from a dead crow found in Statistics: The infection rate was calculated as the Bronx, New York City, NX during an epizootic the number of infected mosquitoes/total tested in 1999 (Turell et al. 2000) and had been passaged X 100. The dissemination rate was calculated as the once in Vero cell culture. Viral stock suspensions, number of mosquitoes with positive legs/total test- triturated mosquito suspensions, and chicken blood ed x100. The transmission rate was calculated as samples were tested for infectious virus by plaque the number of mosquitoes transmitting virus by bite assay on African green monkey kidney (Vero) cells (chickens were viremic when bled the day after the as described by Gargan et al. (1983), except that transmission attempt)/the number of mosquitoes the 2nd overlay, containing neutral red, was added that fed on these chickens. Infection, dissemination, by chi- 2 days after the lst overlay. and transmission rates were compared as appropriate and sig- Vector competence studies: Mosquitoes, 4 to 5 square or Fisher exact tests were determined at the 95Vo days old, were allowed to feed on a chicken (Gallus nificant differences level (SAS Institute Inc. 1999). A 1-way gallus L.) that had been inoculated subcutaneously confidence analysis of variance (ANOVA) was used to test for 24 or 48 h earlier with 0.1 ml of a suspension con- differences in the mean titer (log transformed) of taining l0a' plaque-forming units (PFU) of WN. WN ingested among the strains. The means (1og When most of the mosquitoes in a carton had fed transformed) from the study of viral replication in (:15 min), the chicken was transferred to a 2nd the bodies of infected mosquitoes were subjected carton containing a different strain of mosquitoes. to 2-way ANOVA to evaluate the main effects for This was repeated until all 4 strains of mosquitoes strain and day after oral exposure and the interac- had an opportunity to feed upon the same chicken. tion term. For terms found to be significant (ot : Immediately after mosquito feeding, a 0.1-ml blood 0.05) by ANOVA, the means were separated by sample was obtained from the jugular vein of each Duncan's multiple range test (SAS Institute Inc. chicken and diluted in 0.9 ml of diluent (lOVo heat- 1999). inactivated fetal bovine serum in Medium 199 (In- vitrogen, Carlsbad, CA) with Earle's salts, NaHCO3, and antibiotics) plus 10 units of heparin per milli- RESULTS viremia at the time of mos- liter to determine the All strains of Ae. albopictus were susceptible to quito feeding. Engorged mosquitoes were trans- infection with WN at both viral titers tested (Table ferred to 3.8-liter cartons with netting over the open 1). Susceptibility to infection for each strain signif- end and maintained in an incubator as described icantly increased with viral titer (1'> 5.4, df : I, above. Four days after the infectious blood meal, P < O.O2). Additionally, within viral titer levels, an oviposition substrate was added to each cage. susceptibility to infection was associated with strain To determine transmission rates, some of the tested (12 > 11.6, df : 3, P < 0.009). At the higher mosquitoes that had taken an infectious blood meal viral titer, infection rates of the TAMU (96Vo) and were individually allowed to refeed on a 2-day-old OAHU (937o) strains were significantly higher (X' chicken 13 days after the initial infectious blood > 10.0, df : l, P < 0.002) than infection rates of meal.
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