West Nile Virus Infection in Mosquitoes, Birds, Horses, and Humans, Staten Island, New York, 2000.West Nile West Nile may refer to:
New York, Middle Atlantic state of the United States. It is bordered by Vermont, Massachusetts, Connecticut, and the Atlantic Ocean (E), New Jersey and Pennsylvania (S), Lakes Erie and Ontario and the Canadian province of , where 10 neurologic illnesses among humans and 2 among horses occurred. WN virus was isolated from Aedes vexans, Culex Culex /Cu·lex/ (ku´leks) a genus of mosquitoes found throughout the world, many species of which are vectors of disease-producing organisms. Cu·lex n. pipiens, Cx. salinarius, Ochlerotatus triseriatus, and Psorophora ferox, and WN viral RNA RNA: see nucleic acid. RNA in full ribonucleic acid One of the two main types of nucleic acid (the other being DNA), which functions in cellular protein synthesis in all living cells and replaces DNA as the carrier of genetic was detected in Anopheles Anopheles: see mosquito. punctipennis. An elevated weekly minimum infection rate (MIR) for Cx. pipiens and increased dead bird density were present for 2 weeks before the first human illness occurred. Increasing mosquito MIRs and dead bird densities in an area may be indicators of an increasing risk for human infections. A transmission model is proposed involving Cx. pipiens and Cx. restuans as the primary enzootic en·zo·ot·ic adj. Prevalent among or restricted to animals of a specific geographic area. Used of a disease. n. An enzootic disease. enzootic peculiar to or present constantly in a location. See also endemic. and epizootic ep·i·zo·ot·ic adj. Affecting a large number of animals at the same time within a particular region or geographic area. Used of a disease. ep vectors among birds, Cx. salinariusas the primary bridge vector for humans, and Aedes/Ochlerotatus spp. as bridge vectors for equine infection. During the 1999 outbreak of West Nile (WN) virus in the greater New York City New York City: see New York, city. New York City City (pop., 2000: 8,008,278), southeastern New York, at the mouth of the Hudson River. The largest city in the U.S. (NYC NYC abbr. New York City NYC New York City ) area, surveillance for virus in mosquito populations did not begin until early September, when the epidemic among humans had already peaked (1). From September through October 1999, WN virus was isolated from nine NYC mosquito pools, including two pools of Culex pipiens, six pools of unidentified Culex species This is a list of described Culex species around the world, as of 2006. Subspecies have been omitted. There are possibly errors and inaccuracies in this list that stem from the conversion from the source. Please check the original source when in doubt. , and one pool of mixed Cx. pipiens/restuans. The mosquitoes were identified by using morphologic characters. Subsequent molecular testing of two of the unidentified Culex sp. pools revealed that they were composed of Cx. restuans and Cx. salinarius (2). Evidence of WN virus infection was found in both dead and live wild birds in NYC in the 1999 outbreak, but there was no systematic monitoring of dead bird sightings in the weeks preceding the first human illness or during the human epidemic. In anticipation of a possible return of WN virus during 2000, the NYC Department of Health (NYCDOH NYCDOH New York City Department of Health ) established a citywide network of adult mosquito traps and systematically monitored dead bird sightings as part of a comprehensive program for surveillance, prevention, and control of WN virus in the city. An integrated mosquito management program was initiated throughout the city, which included breeding site elimination, larval larval 1. pertaining to larvae. 2. larvate. larval migrans see cutaneous and visceral larva migrans. control, and public education that encouraged residents to remove mosquito sources from their property and to use personal protective behaviors to avoid mosquito bites. The first dead bird on Staten Island (SI) in 2000 with laboratory evidence of WN virus was found on July 5, and the first mosquitoes with laboratory evidence of WN virus were collected on SI on July 7. By the end of the mosquito-borne disease transmission season, SI had 71% (10/14) of NYC's human cases, as well as 77% (131/170) of mosquito pools and 33% (61/185) of dead birds with laboratory evidence of WN virus. SI, one of the five NYC boroughs, has a surface area of 60.2 square miles (156 square kilometers) and a population of 378,977 (3). The population density is 6,295 persons/square mile, less than the density of the other four boroughs (range by borough: 17,409 to 62,765). SI has 115 acres/square mile of park land, compared with the average 80 acres/square mile in the other four boroughs (range by borough: 54 to 155) (3). This island also has 88% (2,942/3,350 acres) of NYC's freshwater wetlands (GIS Unit, Region 2, New York State Department of Environmental Conservation, unpub, data). During the 1999 WN virus outbreak, SI was the only NYC borough without a human case of WN virus infection. There were no WN virus-infected mosquitoes in the 13 pools collected from SI (a total of 51 adult mosquitoes) October 2-10 (2). The percentage of live wild birds with WN virus antibody in a September 1999 avian serosurvey was 2% (1/43) on SI, compared with 5% (1/20) in Brooklyn and 51% (128/253) in Queens (N. Komar, pers. commun.). Among the eight WN virus-infected dead birds found on SI during 1999, seven were found during October. We summarize key entomologic en·to·mol·o·gy n. The scientific study of insects. en  to·mo·log , avian, human, and equine surveillance
findings from SI from the 2000 outbreak of WN virus, the first year of
prospective surveillance for WN virus infection among mosquitoes, birds,
horses, and humans in NYC. The results from SI are compared with the
other NYC boroughs.Methods Adult Mosquito Collection Adult mosquitoes were collected one night per week from May 2 through November 17 by using CDC See Control Data, century date change and Back Orifice. CDC - Control Data Corporation miniature light traps baited with dry ice and CDC gravid gravid /grav·id/ (grav´id) pregnant. grav·id adj. Carrying eggs or developing young. gra·vid traps at 21 locations on SI (Figure 1) and 80 locations in the other boroughs. During August 14 to September 2, adult mosquitoes were collected 5-7 nights per week on SI as part of an evaluation of the efficacy of adult mosquito control. All traps were set in the late afternoon and evening and retrieved the following morning. Specimens were immediately frozen with dry ice. [ILLUSTRATION OMITTED] Adult mosquitoes were identified and sorted to species whenever possible. If the condition of a specimen did not permit species identification, specimens were grouped as Cx. pipiens/restuans or by genus alone. Up to 50 adult mosquito specimens were pooled (pools of Cx. salinarius had up to 100 specimens) by trap site and date. Mosquito pools collected from May 2 to June 2 were submitted to the Centers for Disease Control and Prevention Centers for Disease Control and Prevention (CDC), agency of the U.S. Public Health Service since 1973, with headquarters in Atlanta; it was established in 1946 as the Communicable Disease Center. laboratory in Fort Collins, Colorado The City of Fort Collins, a home rule municipality situated on the Cache la Poudre River along the Colorado Front Range, is the county seat and most populous city in Larimer County, Colorado. , and pools from June 3 to November 17 were submitted to the Arbovirus arbovirus Any of a large group of viruses that develop in arthropods (chiefly mosquitoes and ticks). The name derives from “arthropod-borne virus.” The spheroidal virus particle is encased in a fatty membrane and contains RNA; it causes no apparent harm to the Laboratory of the New York State Department of Health (NYSDOH NYSDOH New York State Department of Health ) for testing. Minimum infection rate (MIR) was used as the index of virus activity in mosquito populations. MIR is calculated as the number of WN virus-positive pools per number of adult mosquitoes tested and is expressed as the number positive per 1,000 tested. Weekly MIRs were calculated for each species collected on SI and the other boroughs. Mosquito data include only those specimens that were sorted and tested as of December 2000. Dead Bird Reporting and Collection Dead bird reports were taken from the public by two systems. An interactive voice-response telephone system allowed callers to leave detailed information about the bird(s) being reported in a recorded message. Reports could also be entered onto a form on the NYCDOH web site. In both systems, the reporter was asked to provide the date the bird was initially found; its exact location, including street address, borough (county), and zip code zip code System of postal-zone codes (zip stands for “zone improvement plan”) introduced in the U.S. in 1963 to improve mail delivery and exploit electronic reading and sorting capabilities. ; species; and cause of death (if known). The density of reported dead birds per square mile of surface area was determined by week for SI and the other boroughs. Dead bird reports were reviewed before data entry; those meeting predetermined pre·de·ter·mine v. pre·de·ter·mined, pre·de·ter·min·ing, pre·de·ter·mines v.tr. 1. To determine, decide, or establish in advance: criteria were collected for WN virus testing. Collection was limited to birds recently dead (found in the previous 24 to 48 hours) and in relatively good condition (e.g., little or no decay). The primary criterion for collection was the species of bird. Initially only crows (American or Fish), sparrows, Blue Jays, or any cluster of five or more birds were collected for testing. Collection was expanded to include other species, resources permitting, if they were in good condition. Collection of other species focused on raptors (especially Merlins and American Kestrels) or species not typically reported (e.g., Black Skimmer black skimmer n. A skimmer (Rynchops niger) of North and South America that is black above and white below and has a scissorlike bill, bright red legs and feet, and dark brown eyes with vertical pupils. , Belted Kingfisher). Collected birds were sealed in plastic bags and stored with freezer packs in the field. All specimens were submitted to the Wildlife Pathology Unit of the New York State Department of Environmental Conservation for necropsy necropsy /nec·rop·sy/ (nek´rop-se) examination of a body after death; autopsy. nec·rop·sy n. See autopsy. necropsy examination of a body after death. See also autopsy. ; tissue specimens were submitted to the Arbovirus Laboratory of the NYSDOH for WN virus testing. Laboratory Testing of Mosquitoes and Birds Adult mosquito pools and avian tissues were tested for WN virus with one set of primers/probes by real-time reverse transcription-polymerase chain reaction (RT-PCR RT-PCR reverse transcriptase-polymerase chain reaction. See PCR1. ) (TaqMan, ABI Abi (ā`bī) [short for Abijah], in the Bible, King Hezekiah's mother. (Application Binary Interface) A specification for a specific hardware platform combined with the operating system. Prism 7700 Sequence Detector, Applied Biosystems Applied Biosystems, Inc. (formerly NASDAQ: ABIO) is the original name of a pioneer biotechnology company founded in 1981 in Foster City, California, among the Silicon Valley cities of the southern San Francisco Bay Area. , Foster City, CA). Confirmatory tests were performed by using a second TaqMan primer/probe set, standard RT-PCR, virus isolation in cell culture, and immunofluorescence Immunofluorescence A technique that uses a fluorochrome to indicate the occurrence of a specific antigen-antibody reaction. The fluorochrome labels either an antigen or an antibody. assays (avian tissues). A sample was confirmed positive when at least two different tests were positive. Details on virus testing are described elsewhere (4,5). Human and Equine Case Surveillance NYCDOH conducted citywide enhanced passive and active hospital-based physician hospital-based physician A physician who provides 'clinical support' for Pt management, performing medical services within a hospital/health center Examples Radiologists, anesthesiologists, pathologists, ER physicians– and laboratory surveillance for human WN virus infections, including all three acute-care hospitals on SI. Additional details on human surveillance are described elsewhere in this journal by Weiss et al. (6). Surveillance for equine illnesses was by enhanced passive surveillance. Additional details regarding equine surveillance are described elsewhere in this journal by Trock et al. (7). Results Adult Mosquito Collection and Testing A total of 24,068 adult mosquitoes from 23 species were tested in 967 pools from SI; 131 pools from 6 species had laboratory evidence of WN virus. NYSDOH reported WN virus isolation from Aedes vexans, Cx. pipiens, Cx. salinarius, Ochlerotatus triseriatus, and Psorophora ferox, and WN viral RNA detection in Anopheles punctipennis (8). During the same period, a total of 51,044 adult mosquitoes from 26 species were tested in 1,958 pools collected from the other boroughs; 39 of these pools had laboratory evidence of WN virus (Table). These are the first reports of Ae. albopictus and Cx. erraticus from New York State.
Table. Adult mosquitoes collected and tested from New York City
(NYC), as of December 2000(a)
No. of mosquitoes tested
Genus Sp. Staten Other All
Island boroughs NYC
Aedes & Ochlerotatus species 351 1,284 1,635
Aedes albopictus 90 90
vexans 2,497 3,215 5,712
Anopheles crucians 11 2 13
punctipennis 47 3 50
quadrimaculatus 44 44
species 16 37 53
Coquillettidia perturbans 35 3,010 3,045
species 6 6
Culex erraticus 4 4
pipiens 4,820 15,231 20,051
pipiens / restuans 2,554 11,190 13,744
restuans 439 2,480 2,919
salinarius 10,057 7,687 17,744
territans 28 45 73
species 2,242 3,502 5,744
Ochlerotatus canadensis 21 277 298
cantator 14 97 111
excrucians 2 2
intrudens 21 21
japonicus 2 2
sollicitans 33 1,699 1,732
taeniorhynchus 1 118 119
triseriatus 592 180 772
trivittatus 193 784 977
Psorophora ferox 39 19 58
columbiae
species 1 1
Uranotaenia sapphirina 28 28
Unidentified, damaged 64 64
Total 24,074 51,044 75,106
No. of positive pools
Genus Sp. Staten Other All
Island boroughs NYC
Aedes & Ochlerotatus species 1 1
Aedes albopictus
vexans 2 2 4
Anopheles crucians
punctipennis 1 1
quadrimaculatus
species
Coquillettidia perturbans
species
Culex erraticus
pipiens 55 19 74
pipiens / restuans 24 9 33
restuans
salinarius 28 4 32
territans
species 16 4 20
Ochlerotatus canadensis
cantator 1 1
excrucians
intrudens
japonicus
sollicitans
taeniorhynchus
triseriatus 3 3
trivittatus
Psorophora ferox 1 1
columbiae
species
Uranotaenia sapphirina
Unidentified, damaged
Total 131 39 170
(a) Pools were collected by the New York City Department of Health,
the Centers for Disease Control and Prevention, the National Park
Service, and the U.S. Army.
Laboratory evidence of WN virus was first detected from mosquitoes in a Cx. pipiens pool collected July 7 and in a Cx. salinarius pool collected July 17, both from SI. The first human patient on SI became ill on July 20. Additional human cases on SI had onset of disease between July 28 and September 2. Human cases occurred when the MIR among Cx. pipiens and Cx. pipiens/restuans ranged from approximately 5 to 16/1,000 (July 7 to September 22) and the MIR among Cx. salinarius was at least 4/1,000 (6 of 7 weeks from July 15 to September 1). The MIR among Cx. salinarius peaked at 9/1,000 in the week ending August 11 (Figure 2). [GRAPH OMITTED] Dead Bird Reports and Testing Overall, 14,849 dead birds were reported in NYC during 2000, including 4,910 (33%) from SI. Of the SI birds, 235 (4.8%) were collected and submitted for testing; 60 (26%) had laboratory evidence of WN virus. These included 45 American Crows, 5 Blue Jays, 2 Snowy Owls, and 1 each of the following species: American Kestrel kestrel Any of several birds of prey (genus Falco) known for hovering while hunting. Kestrels prey on large insects, birds, and small mammals. The male is more colourful than the female. Kestrels are mainly Old World birds, but one species, the American kestrel (F. , Canada Goose Canada goose Brown-backed, light-breasted goose (Branta canadensis) with a black head and neck and white cheeks. Subspecies vary in size, from the 4.4-lb (2-kg) cackling goose to the 14.3-lb (6.5-kg) giant Canada goose, which has a wingspread of up to 6.6 ft (2 m). , Common Grackle common grackle n. A large grackle (Quiscalus quiscula) of eastern North America, having iridescent blackish-purple plumage and a long, wedge-shaped tail. , Fish Crow fish crow n. A crow (Corvus ossifragus) native to the coastal regions and rivers of the eastern United States. , Greater Black-backed Gull, Mourning Dove mourning dove Species (Zenaida macroura) of pigeon (family Columbidae), the common wild pigeon of North America. They have long, pointed tails, and the sides of the neck are violet and pink. Their name comes from their call's haunting, mournful tone. , Northern Mockingbird The Northern Mockingbird, Mimus polyglottos, is the only mockingbird commonly found in North America. The Northern Mockingbird breeds in southeastern Canada, the United States, northern Mexico, the Bahamas, Cayman Islands and the Greater Antilles. , and sparrow. Density of total dead birds per square mile on SI began to increase the week ending July 7 and peaked at [is greater than] 14 dead birds/ square mile per week during the week ending July 21. The density of dead birds remained [is greater than] 5/square mile until the week ending September 1. This period of increased weekly den-sity of dead birds coincided with the period of elevated MIRs among Cx. pipiens, Cx. pipiens/restuans, and Cx. salinarius (Figure 2). Human and Equine Cases Ten human cases of neurologic WN virus infection were reported from SI, and four cases were reported from three other boroughs. Onset of illness for the SI cases ranged from July 20 to September 2 and from August 15 to September 13 for the other boroughs. Four confirmed equine cases were reported, two on SI (onset August 17 and September 8) and two from another borough (onset August 27 and October 1). Conclusion All 10 human infections with WN virus on SI in 2000 occurred when the weekly density of dead birds and mosquito MIRs was elevated. Dead bird density increased to three dead birds/square mile and the MIR for Cx. pipiens and Cx. pipiens/restuans increased to 8-14/1,000 mosquitoes before the first human case was reported. Monitoring dead bird density and mosquito MIRs may detect increased WN viral activity and predict when the risk of human infection with WN virus is increased. The first human patient on SI had onset of symptoms on July 20; if one assumes a 3- to 15-day incubation period incubation period n. 1. See latent period. 2. See incubative stage. Incubation period for WN virus (9), exposure to a WN virus-infected mosquito would have occurred between July 5 and July 17. WN virus was first detected in a pool of Cx. pipiens collected on July 7 and in a Cx. salinarius pool collected on July 17 from different sites approximately 2 miles from the residence of the first human case. Additional human cases on SI had onset of disease between July 28 and September 2, with exposure to a WN virus-infected mosquito estimated to be between July 13 and August 29. MIRs remained elevated during this period. Based on the observations on SI, we propose a model of transmission that may be applicable to similar habitats elsewhere in the northeastern United States. Cx. pipiens and Cx. restuans appear to serve as the primary enzootic and epizootic vectors among birds. Blood-meal analyses of mosquitoes collected in NYC during 2000 show that Cx. pipiens feeds predominantly on birds (Charles Apperson, pers. commun.), consistent with an earlier observation by Spielman (10). This interaction appears to amplify the amount of virus circulating in spring and early summer. Cx. salinarius appears to serve as the bridge vector for human transmission. This mosquito has also been hypothesized as a bridge vector for human transmission of eastern equine encephalomyelitis Eastern equine encephalomyelitis see encephalomyelitis. virus (11). Aedes/Ochlerotatus spp. appear to be infected later in the season and serve as bridge vectors for horses. There are several important limitations to the observations reported in this paper. The data presented reflect a single year of data, and additional surveillance data over time will be needed to determine if there is a consistent correlation between increased dead bird density, elevated mosquito MIRs, and human case onset. The advance warning provided by dead bird and mosquito data appears to be limited to no more than 10 days. While dead bird reports can be monitored daily and a weekly dead bird density can be quickly determined, MIR data require the labor-intensive and time-consuming steps of pooling by species and laboratory testing. The usefulness of MIR data depends on timely completion of these tasks. Polymerase chain reaction polymerase chain reaction (pŏl`ĭmərās') (PCR), laboratory process in which a particular DNA segment from a mixture of DNA chains is rapidly replicated, producing a large, readily analyzed sample of a piece of DNA; the process is (PCR PCR polymerase chain reaction. PCR abbr. polymerase chain reaction Polymerase chain reaction (PCR) ) was the primary method of laboratory testing of birds and mosquitoes from SI, and viral culture viral culture A test in which a specimen–eg, throat swab, sputum, stool, CSF, urine, from a Pt is placed in live cells; various viruses–eg, adenovirus, enterovirus, herpes simplex, measles, mumps, myxovirus, paramyxovirus, rhinovirus, rubella, was not performed to confirm the presence of live WN virus in all specimens. The interpretation of PCR results without viral confirmation requires caution. However, vector competence for WN virus transmission has been demonstrated for Ae. vexans, Cx. pipiens (12), Cx. salinarius (Michael Turell, unpub. data), and Oc. triseriatus (Michael Turell, pers. commun.). These four species made up 98% (112/ 114) of the positive mosquito pools sorted to species from SI reported in this paper. Vector competence has not been determined for Ps. ferox or An. punctipennis. Dead bird data are limited in that avian mortality is not an established surveillance method for which baseline rates are known. We are unable to compare the number of dead birds reported on SI in 2000 with a prior year's data. Furthermore, public interest in reporting dead birds could wane over time, limiting the usefulness of this surveillance technique. The dead bird densities shown in this paper were calculated at the borough (county) level, and analysis at smaller geographic units may detect more focal areas of transmission that are at greater risk for human infection than surrounding locations. Additional surveillance methods, e.g., live bird surveillance or use of sentinel animals, may provide a more timely warning of increasing risk of human WN viral infection viral infection, n an infection by a pathogenic virus. A virus acts on the cell nucleus, taking over the genetic material within the nucleus and replicating itself. . Acknowledgments Among the hundreds of coworkers at our institutions who contributed to the West Nile virus West Nile virus, microorganism and the infection resulting from it, which typically produces no symptoms or a flulike condition. The virus is a flavivirus and is related to a number of viruses that cause encephalitis. response, the authors thank Ward Stone for avian tissue processing, Jason Thomas Jason Thomas (born ca. 1974) is a former U.S. Marine who helped rescue people after the September 11, 2001 attacks. He helped find a pair of Port Authority Police officers buried in the rubble of the World Trade Center. and Colonel Charles Cannon Charles Reginald Lionel Cannon (November 24, 1866—1952) was a politician in Manitoba, Canada. He served in the Legislative Assembly of Manitoba from 1922 to 1927, and was a cabinet minister in the government of John Bracken. for providing adult mosquito collection and testing data, Lisa Mill for assistance with adult mosquito sorting, Marci Layton for providing comments on the draft, Susan Resnick for preparation of the map, Varner Demary for supervising adult mosquito collection, the staff of the New York State Department of Health Arboviral Laboratory for testing avian tissues and mosquito pools, and Kristy Gottfried, Kristy Burkhalter, and Amy Kerst for assistance in testing mosquito pools. Dr. Kulasekera is a research scientist in charge of the mosquito surveillance program in New York City. Her research interests include ecologic and evolutionary interactions among mosquitoes and the pathogens they transmit. References (1.) Centers for Disease Control and Prevention. Outbreak of West Nile-like viral encephalitis--New York, 1999. MMWR MMWR Morbidity & Mortality Weekly Report Epidemiology A news bulletin published by the CDC, which provides epidemiologic data–eg, statistics on the incidence of AIDS, rabies, rubella, STDs and other communicable diseases, causes of mortality–eg, Morb Mortal Wkly Rep 1999;48:846. (2.) Nasci RN, White DJ, Stirling H, Oliver JA, Daniels TJ, Falco RC, et al. West Nile virus isolates from mosquitoes in New York and New Jersey, 1999. Emerg Infect Dis 2001;7:626-30. (3.) City of New York. The 1998-99 green book, official directory of the City of New York. 73rd ed. New York: City of New York; 1998:607-8. (4.) Kramer LD, Bernard KA. West Nile virus tissue tropisms in birds and mammals. Ann NY Acad Sci 2001; in press. (5.) Shi P-Y, Kauffman EB, Ren P, Felton A, Tai JH, Dupuis II AP, et al. High throughput detection of West Nile virus RNA. J Clin Microbiol 2001;39:1264-71. (6.) Weiss D, Carr D, Kellachan J, Tan C, Phillips M, Bresnitz E, et al. Clinical findings of West Nile virus infection in hospitalized patients, New York and New Jersey, 2000. Emerg Infect Dis 2001;7:654-8. (7.) Trock SC, Meade BJ, Glaser AL, Ostlund EN, Lanciotti RS, Cropp BC, et al. West Nile virus outbreak among horses in New York State, 1999 and 2000. Emerg Infect Dis 2001;7:745-7. (8.) Bernard KA, Maffei JG, Jones SA, Kauffman EB, Ebel GD, Dupuis AP, et al. West Nile virus infection in birds and mosquitoes in New York State, 2000. Emerg Infect Dis 2001;7:679-85. (9.) Olejnik E. Infectious adenitis adenitis /ad·e·ni·tis/ (ad?e-ni´tis) inflammation of a gland. Bartholin adenitis inflammation of the greater vestibular gland (Bartholin's gland) resulting from acute infection of the gland. transmitted by Cx. molestus. Bulletin of the Research Council of Israel 1952; 2:210-11. (10.) Spielman A. Population structure in the Cx. pipiens complex of mosquitoes. Bull World Health Organ 1967;37:271-6. (11.) Vaidyanathan R, Edman JD, Cooper LA, Scott TW. Vector competence of mosquitoes (Diptera: Culicidae) from Massachusetts for a sympatric sym·pat·ric adj. Ecology Occupying the same or overlapping geographic areas without interbreeding. Used of populations of closely related species. isolate of eastern equine encephalomyelitis virus. J Med Entomol 1997;34:346-52. (12.) Turell MJ, O'Guinn ML, Dohm DJ, Jones JW. Vector competence of North American North American named after North America. North American blastomycosis see North American blastomycosis. North American cattle tick see boophilusannulatus. mosquitoes (Diptera: Culicidae) for West Nile virus. J Med Entomol 2001;38:130-4. Varuni L. Kulasekera,(*) Laura Kramer,([dagger]) Roger S. Nasci,([double dagger]) Farzad Mostashari,([sections]) Bryan Cherry,(*) Susan C. Trock,([paragraph]) Carla Glaser,(*) and James R. Miller(*) (*) New York City Department of Health, New York, New York, USA; ([dagger]) New York State Department of Health, Albany, New York For other uses, see Albany. Albany is the capital of the State of New York and the county seat of Albany County. Albany lies 136 miles (219 km) north of New York City, and slightly to the south of the juncture of the Mohawk and Hudson Rivers. , USA; ([double dagger]) Centers for Disease Control and Prevention, Fort Collins, Colorado, USA; ([sections]) OutbreakDetect Inc., New York, New York, USA; and ([paragraph]) Cornell University, Ithaca, New York
For other places or objects named Ithaca, see Ithaca (disambiguation). , and New York State Department of Agriculture and Markets, Albany, New York, USA Address for correspondence: Varuni Kulasekera, Room 619, CN 32P, New York City Department of Health, 125 Worth Street, New York, New York 10013, USA; fax: 212-442-5215; e-mail: vkulasek@health.nyc.gov |
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