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West Nile Virus Isolates from Mosquitoes in New York and New Jersey, 1999.


An outbreak of encephalitis encephalitis (ĕnsĕf'əlī`təs), general term used to describe a diffuse inflammation of the brain and spinal cord, usually of viral origin, often transmitted by mosquitoes, in contrast to a bacterial infection of the meninges  due to West Nile West Nile may refer to:
  • West Nile virus
  • West Nile region in Uganda
 (WN) virus occurred in 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.
 and the surrounding areas during 1999. Mosquitoes were collected as part of a comprehensive surveillance program implemented to monitor the outbreak. More than 32,000 mosquitoes representing 24 species were tested, and 15 WN virus isolates were obtained. Molecular techniques were used to identify the species represented in the WN virus-positive mosquito pools. Most isolates were from pools containing 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 mosquitoes, but several pools contained two or more 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.
.

In late August 1999, an outbreak of human encephalitis was detected in New York City (NYC NYC
abbr.
New York City


NYC New York City
) (1). The first cases occurred in a small area in northern Queens and were immunoglobulin M immunoglobulin M
n. Abbr. IgM
The class of antibodies found in circulating body fluids and the first antibodies to appear in response to an initial exposure to an antigen.
 seropositive seropositive /se·ro·pos·i·tive/ (-poz´i-tiv) showing positive results on serological examination; showing a high level of antibody.

se·ro·pos·i·tive
adj.
 against St. Louis encephalitis St. Louis encephalitis

see St. Louis encephalitis.
 (SLE SLE systemic lupus erythematosus.

SLE
abbr.
systemic lupus erythematosus


Systemic lupus erythematosus (SLE) 
) virus. The etiologic agent was West Nile (WN) virus (2,3), a member of the Japanese encephalitis Japanese Encephalitis Definition

Japanese encephalitis is an infection of the brain caused by a virus. The virus is transmitted to humans by mosquitoes.
 virus complex (genus Flavivirus, family Flaviviridae), which includes other mosquito-transmitted human pathogens such as Japanese encephalitis virus, SLE virus, Murray Valley encephalitis virus Murray Valley encephalitis virus (MVEV) is a zoonotic flavivirus endemic to northern Australia and Papua New Guinea. It is the causal agent of Murray Valley encephalitis (previously known as Australian encephalitis) and in humans can cause permanent neurological disease or death. , and Kunjin viruses (4). Both SLE virus, which is a native North American North American

named after North America.


North American blastomycosis
see North American blastomycosis.

North American cattle tick
see boophilusannulatus.
 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
, and WN viruses are zoonotic Zoonotic
A disease which can be spread from animals to humans.

Mentioned in: Zoonosis
 agents maintained in a transmission cycle involving bird and mosquito species (4,5).

Outbreak investigations identified human and animal cases, virus-positive dead birds, seropositive live birds, and virus-positive mosquitoes, indicating widespread virus transmission throughout the NYC metropolitan area (6,7). Sixty-two laboratory-confirmed human cases with clinical illness occurred (46 in NYC, 15 in surrounding suburbs in Westchester and Nassau counties, and 1 in a Canadian tourist who visited NYC) (8). The earliest detected onset of human illness occurred during the first week of August and the latest during the third week of September 1999 (2). In this report, we describe the mosquito surveillance program conducted in response to the outbreak and discuss mosquito species associated with WN virus transmission in 1999.

Materials and Methods

Surveillance designed to monitor mosquito populations associated with the outbreak and determine the species and proportion of mosquitoes carrying the virus was initiated in NYC and surrounding counties during the first 2 weeks of September. NYC and most surrounding counties had not maintained systematic mosquito surveillance and control programs before this outbreak. As a result, no information was available about the density or distribution of mosquito species in the area (1). The exceptions were Nassau and Suffolk counties, NY, and all counties in New Jersey (NJ), where comprehensive mosquito control programs, including surveillance for eastern equine encephalitis Eastern equine encephalitis A rare, sporadic, and aggressive enzootic infection by a single-stranded RNA Togavirus that primarily affects birds Vector Ornithophilic mosquito, Culiseta melanura  (EEE EEE eastern equine encephalomyelitis.

EEE

eastern equine encephalomyelitis.
) virus activity, had been in effect for many years. As widespread virus transmission became apparent, mosquitoes were collected from a broader geographic area. Existing mosquito control programs participated by expanding mosquito sampling and providing specimens for testing.

Mosquitoes were collected from September 2, 1999, through October 29, 1999. Some Culex species mosquitoes collected earlier in the season as part of long-term EEE virus monitoring programs were provided by Suffolk and Nassau counties to assess evidence of infection in mosquitoes before the onset of human cases. Carbon dioxide-baited CDC See Control Data, century date change and Back Orifice.

CDC - Control Data Corporation
 miniature light traps (9) or traps of similar design were used to collect host-seeking adult female mosquitoes of various species. CDC gravid gravid /grav·id/ (grav´id) pregnant.

grav·id
adj.
Carrying eggs or developing young.



gra·vid
 traps (10) or traps of similar design were used to collect gravid female mosquitoes (i.e., those that had taken a blood meal and were searching for a site to lay eggs) of the genus Culex. Although WN virus has been isolated from ([is greater than]) 40 mosquito species and several species of ticks (11), Culex species mosquitoes have been frequently associated with transmission of SLE and WN viruses (4,12,13).

Mosquitoes were placed in labeled tubes, frozen and held at -70 [degrees] C, and shipped 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. , 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. . The specimens were identified to species if possible, but the condition of certain morphologically similar Culex mosquitoes often prevented this. Morphologic characteristics essential for accurate species identification are often damaged during mosquito collection and shipping (and as a result of natural aging of mosquitoes). Therefore, many specimens were only identified to the level of genus or to a species group (e.g., Cx. pipiens/ restuans group, which includes the morphologically similar Cx. pipiens and Cx. restuans species). All specimens, including those that appeared to contain blood meals or partially digested blood meals, were tested for virus. Therefore, the virus infection rate in the mosquito population reflects the proportion of mosquitoes that had contacted a viremic host. Specimens were grouped into pools of 50 (by species, date, and location of collection) and were tested for virus. Every mosquito pool was tested by a Vero cell Vero cells are lineages of cells used in cell cultures.[1]

The Vero lineage was isolated from kidney epithelial cells extracted from African green monkey (Cercopithecus aethiops).
 plaque assay (14), which is sensitive to all North American mosquito-transmitted pathogenic viruses and many nonpathogenic mosquito-transmitted viruses. After WN virus was determined to be the etiologic agent, a WN virus-specific reverse transcriptase-polymerase chain reaction (RT-PCR RT-PCR

reverse transcriptase-polymerase chain reaction. See PCR1.
) assay (15) was used in conjunction with the Vero cell plaque assay to detect and identify WN virus in mosquito pools. Other viruses isolated in the plaque assay were identified by virus-specific RT-PCR (R. Lanciotti, unpub, data). The identity of the mosquitoes in virus-positive pools was subsequently determined or verified by species-diagnostic PCR PCR polymerase chain reaction.

PCR
abbr.
polymerase chain reaction


Polymerase chain reaction (PCR) 
 (16). This technique, based on interspecific in·ter·spe·cif·ic  
adj.
Arising or occurring between species.



interspecific also interspecies  

Arising or occurring between species.

Adj. 1.
 nucleic acid nucleic acid, any of a group of organic substances found in the chromosomes of living cells and viruses that play a central role in the storage and replication of hereditary information and in the expression of this information through protein synthesis.  sequence variation, identifies Cx. pipiens, Cx. restuans, or Cx. salinarius (in combination or alone) in a pool of 50 mosquitoes.

Results

During the surveillance program, 32,814 mosquitoes representing 25 species were collected and tested for WN virus in 1,853 pools (Table 1). More than half of mosquitoes tested (18,016) were in the genus Culex; most of these could not be identified to species but were likely Cx. pipiens or Cx. restuans. In the remaining specimens, the predominant species were the floodwater flood·wa·ter  
n.
The water of a flood. Often used in the plural.

floodwater naguas fpl (de la inundación)

floodwater n
 mosquitoes Aedes vexans and Ae. trivittatus. The collection period, number of Culex mosquitoes, and number of other mosquito species tested for each of the 10 NY and 10 NJ counties providing specimens are listed in Table 2. The number collected and tested was not a good representation of the relative population density of Culex and other species mosquitoes because sampling was not consistent across participating counties. The total number collected was higher in areas where sampling was more intense. The numbers of Culex and other species within a county were representative of the relative abundance of various mosquito larval larval

1. pertaining to larvae.

2. larvate.


larval migrans
see cutaneous and visceral larva migrans.
 habitats where mosquito traps were placed (e.g., permanent water sites appropriate for Cx. pipiens and Cx. restuans development vs. floodwater habitats appropriate for Ae. vexans and Ae. trivittatus).
Table 1. Mosquito species identification by morphologic
characteristics, New York and New Jersey, 1999

Genus                          Species             Total

Aedes                albopictus                         8
                     canadensis                        26
                     cantator                          55
                     cinereus                         426
                     japonicus                         64
                     sollicitans                      178
                     sticticus                        175
                     taeniorhynchus                   187
                     triseriatus                      132
                     trivittatus                    3,274
                     vexans                         7,956
                     unidentified Aedes sp.           901
Anopheles            bradleyi                           1
                     punctipennis                      23
                     quadrimaculatus                   77
                     walkeri                           32
                     unidentified Anopheles sp.        12
Coquillettidia       perturbans                       155
Culiseta             melanura                         587
Culex                erraticus                          4
                     pipiens                          511
                     pipiens / restuans             4,686
                     restuans                         215
                     salinarius                     1,866
                     territans                          8
                     unidentified Culex sp.        10,726
Psorophora           ferox                            245
                     unidentified Psorophora sp.        6
Uranotaenia          sapphirina                        31
Unidentified genus   unidentified mosquito sp.        256
Total                                              32,814
Table 2. Mosquito species tested for West Nile virus, New York and New
Jersey, 1999

                                                    No. tested
                              Collection dates      Culex   Other
                              From       Through     sp.     sp.
New York counties (borough)
  Bronx(a)                    9/2/99     10/26/99     166   4,679
  Kings (Brooklyn)(a)         9/11/99    10/26/99     122      24
  New York (Manhattan)        9/11/99    10/26/99   1,344      93
  Queens(a)                   9/10/99    10/26/99   6,245     156
  Richmond (Staten Island)    10/2/99    10/26/99      18      38
  Nassau(a)                   8/19/99    10/22/99   1,301     846
  Orange                      9/13/99    9/13/99       80      16
  Rockland                    9/13/99    10/5/99      171   1,877
  Suffolk(a)                  6/8/99     10/20/99   6,849   1,217
  Westchester(a)              9/8/99     10/19/99     334   1,206
New Jersey counties
  Bergen                      9/22/99    10/20/99      48     328
  Burlington(b)               10/4/99    10/26/99       0     234
  Camden(b)                   10/4/99    10/25/99       0      53
  Cape May(b)                 9/15/99    10/30/99       0      90
  Essex                       9/24/99    10/12/99      18     521
  Hudson(a)                   9/9/99     10/20/99   1,281   3,255
  Middlesex                   9/24/99    9/30/99        9      25
  Ocean(b)                    9/29/99    9/29/99        0       3
  Salem(b)                    9/29/99    10/28/99       0     142
  Warren                      10/28/99   10/28/99       7       3

(a) Counties in which West Nile virus-infected Culex species
mosquitoes were collected.

(b) Other species tested are primarily Culiseta melanura
collected as part of New Jersey's long-term eastern equine
encephalitis surveillance program.


Suffolk County, NY, was an exception. Total collections in Suffolk County were very large, and Culex species mosquitoes were selectively submitted for testing. Several NJ counties provided mainly Culiseta melanura mosquitoes for testing. This species feeds almost exclusively on birds and is 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.
 vector of EEE virus. These specimens were solicited to determine if WN virus-infected birds were being fed upon as they migrated south in late summer and early fall. WN virus-infected mosquitoes were collected in six NY counties and one NJ county.

WN virus was isolated from 15 pools of mosquitoes (Table 3). All isolates were from Culex species. Identification of the species composition of these pools by molecular techniques indicated that six pools contained exclusively Cx. pipiens and seven contained two or more Culex species (combinations of Cx. pipiens, Cx. restuans, and Cx. salinarius). Two pools contained insufficient material for molecular species identification. The only evidence that another species was involved in WN virus transmission in 1999 was the isolation of WN virus from a pool of Ae. vexans mosquitoes collected on September 14, 1999, in southwestern Connecticut Southwestern Connecticut is a geographic region of the U.S. state of Connecticut. There are no official definitions for this region but generally includes one or more of the following official regions located entirely or partly in the southern part of Fairfield County:
 (7). The earliest WN virus isolates in NY and NJ came from collections made on September 12, 1999, in Queens, Brooklyn, and the Bronx. The latest WN virus isolate came from collections made on October 10, 1999, in Queens and Nassau County. Most isolates were from Queens, which was the location of most human WN-virus infection cases (6).
Table 3. West Nile virus-positive mosquito pools, New York and New
Jersey, 1999

                    Collection      Species(a)         Species(b)
County                date       (morphologic id.)   (molecular id.)

Queens, NY           9/12/99       Culex pipiens       Cx. pipiens
                     9/13/99       Cx. pipiens         Cx. pipiens
                     9/13/99       Cx. species         Cx. pipiens/
                                                         restuans
                     9/19/99       Cx. species         Cx. pipiens
                     9/20/99       Cx. species         Cx. pipiens
                     10/10/99      Cx. pipiens/        insufficient
                                     restuans            sample
Kings (Brooklyn),    9/12/99       Cx. species         Cx. pipiens
  NY
                     9/15/99       Cx. species         Cx. restuans/
                                                         salinarius
Bronx, NY            9/12/99       Cx. species         Cx. restuans/
                                                         salinarius
Nassau, NY           9/29/99       Cx. pipiens         Cx. pipiens
                     10/3/99       Cx. species         Cx. pipiens/
                                                         restuans/
                                                         salinarius
                     10/10/99      Cx. pipiens/        Cx. pipiens/
                                     restuans            restuans/
                                                         salinarius
Suffolk, NY          10/4/99       Cx. species         Cx. restuans/
                                                         salinarius
Westchester, NY      10/1/99       Cx. restuans        Cx. restuans/
                                                         salinarius
Hudson, NJ           9/28/99       Cx. pipiens          insufficient
                                                           sample

(a) Species identification by morphologic characteristics.

(b) Species identification by species-specific polymerase
chain reaction primers.


Other viruses were isolated from mosquitoes during the surveillance program (Table 4). Flanders virus was isolated from 11 pools of Culex species mosquitoes, most of which contained combinations of species. Flanders virus is a widely distributed Adj. 1. widely distributed - growing or occurring in many parts of the world; "a cosmopolitan herb"; "cosmopolitan in distribution"
cosmopolitan

bionomics, environmental science, ecology - the branch of biology concerned with the relations between organisms
 rhabdovirus rhabdovirus

Any of a group of viruses responsible for rabies and vesicular stomatitis (an acute disease of cattle and horses, characterized by blisters in and about the mouth, that resembles foot-and-mouth disease).
 frequently found in birds and bird-feeding mosquitoes and apparently nonpathogenic in vertebrates (17). EEE virus was isolated from a pool of Cs. melanura collected in Burlington County, NJ. Three isolates of a California serogroup virus were obtained from pools of Ae. trivitattus collected in the Bronx and Nassau County, NY. Numerous California serogroup viruses are present in this region of North America North America, third largest continent (1990 est. pop. 365,000,000), c.9,400,000 sq mi (24,346,000 sq km), the northern of the two continents of the Western Hemisphere.  (18). Although these California serogroup isolates were not specifically identified for this study, they are likely trivitattus virus, a generally nonpathogenic member of the California serogroup commonly found in Ae. trivittatus (19).
Table 4. West Nile virus-positive mosquito pools containing viruses
other than West Nile virus, collection location, date, species
composition, and virus identification

                 Collection        Species(a)
County             date         (morphologic id.)

Bronx, NY        9/9/99       Aedes trivittatus
                 9/12/99      Ae. trivittatus
Nassau, NY       10/15/99     Culex pipiens / restuans
                 10/16/99     Ae. trivittatus
Suffolk, NY      6/29/99      Cx. pipiens / restuans
                 6/29/99      Cx. pipiens / restuans
                 7/7/99       Cx. pipiens / restuans
                 7/27/99      Cx. pipiens / restuans
                 8/3/99       Cx. pipiens / restuans
                 8/10/99      Cx. pipiens / restuans
                 8/10/99      Cx. pipiens / restuans
                 8/16/99      Cx. pipiens / restuans
                 9/28/99      Cx. restuans
Hudson, NJ       9/22/99      Cx. pipiens
Burlington, NJ   10/11/99     Culiseta melanura

                    Species(b)
County           (molecular id.)             Virus identification

Bronx, NY        not done                    California serogroup
                 not done                    California serogroup
Nassau, NY       Cx. pipiens/restuans/
                   salinarius                Flanders
                 not done                    California serogroup
Suffolk, NY      Cx. pipiens / restuans      Flanders
                 Cx. restuans                Flanders
                 Cx. pipiens / restuans      Flanders
                 Cx. pipiens / restuans /
                   salinarius                Flanders
                 Cx. pipiens / restuans /
                   salinarius                Flanders
                 insufficient sample         Flanders
                 insufficient sample         Flanders
                 insufficient sample         Flanders
                 Cx. restuans / salinarius   Flanders
Hudson, NJ       Cx. pipiens                 Flanders
Burlington, NJ   not done                    Eastern equine
                                               encephalitis

(a) Species identification by morphologic characteristics.

(b) Species identification by species-specific polymerase chain
reaction primers.


The minimum infection rate (MIR) of WN virus in Culex mosquitoes, expressed as the number infected per 1,000 specimens tested, was calculated by county for the sampling periods (weeks) during which WN virus was isolated from mosquitoes (Table 5). MIR for a given period and location is an indicator of prevalence of virus in the habitat and of transmission intensity and, in many circumstances, is related to the risk for human disease. All Culex mosquitoes collected in a county during a particular week, except Cx. territans, which feeds predominantly on amphibians amphibians

members of the animal class Amphibia. Includes frogs, toads, newts, salamanders and cecilians all capable of living on land or in water.
, were combined to determine the denominator for this value because many of the Culex specimens could not be identified below genus or species levels. As a result, MIR estimates probably underestimate the infection rate for certain Culex species and overestimate the rate for others. MIR for WN virus-infected Culex in this outbreak was 0.7/1,000 to 57.1/1,000, although the 95% confidence intervals are very large around MIR estimates calculated from small sample sizes.
Table 5. West Nile (WN) virus infection rates in Culex species
mosquitoes, New York and New Jersey, 1999

                             #WN        Total                (95%
                             virus-     Culex                Confi-
Sampling                    positive   specimens             dence
period        County         pools     tested(a)   MIR(b)   Interval)

9/12-9/19     Queens          3           820        3.7    (0.8-10.7)
              Kings           2            35       57.1    (7.0-191.6)
               (Brooklyn)
              Bronx           1            48       20.8    (0.5-110.7)
9/19-9/25     Queens          2           862        2.3    (0.3-8.3)
9/26-10/2     Nassau          1           198        5.1    (0.1-27.8)
              Hudson, NJ      1           138        7.2    (0.2-39.7)
              Westchester     1            92       10.8    (2.0-54.5)
10/3-10/9     Nassau          1           214        4.7    (0.1-25.8)
              Suffolk         1           810        1.2    (0.03-6.9)
10/10-10/16   Queens          1          1496        0.7    (0.02-3.7)
              Nassau          1           135        7.4    (0.2-40.6)

(a) Excluding Culex territans.

(b) Minimum infection rate expressed as number infected per
1,000 specimens tested.


Conclusion

Mosquito surveillance, although not implemented until late in the outbreak (well after most transmission to humans that resulted in clinical cases), provided information about transmission dynamics that may prove useful in developing new surveillance systems. Culex mosquitoes, particularly Cx. pipiens, appear primarily responsible for 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
 transmission. Cx. pipiens was quite common in Queens, NY, and other areas where isolates were obtained and transmission activity was documented by avian and human surveillance programs. Cx. restuans and Cx. salinarius were also implicated im·pli·cate  
tr.v. im·pli·cat·ed, im·pli·cat·ing, im·pli·cates
1. To involve or connect intimately or incriminatingly: evidence that implicates others in the plot.

2.
 in virus transmission. Since these species were found only in combination in WN virus-positive pools, their importance is difficult to assess. Cx. pipiens and Cx. restuans ace ornithophilic, feeding mainly on birds and occasionally on mammals (20). Cx. salinarius, which is a pest species common in the region (21), feeds readily on humans and other mammals (20), which suggests that it may be involved in epidemic transmission of WN virus.

Relatively high MIR values in areas where human cases occurred validate use of mosquito-based surveillance to estimate risk for virus transmission to humans. MIRs found in this study are consistent with MIRs calculated for WN virus in mosquitoes reported in other areas. MIR estimates for the primary vector species during WN virus outbreaks range from 0.8/1,000 for Cx. fatigans in India (22) to as high as 25.0/1,000 for Cx. univittatus in South Africa South Africa, Afrikaans Suid-Afrika, officially Republic of South Africa, republic (2005 est. pop. 44,344,000), 471,442 sq mi (1,221,037 sq km), S Africa.  (23). While it is difficult to associate a quantified risk for human disease to an MIR value, evidence from Cx. pipiens-borne SLE outbreaks indicates that widespread transmission to humans is likely when MIR exceeds 3/1,000 but may occur at much lower infection rates (24).

Mosquito-based virus surveillance has its limitations. Adequate estimates of virus distribution and transmission require extensive field and laboratory resources to obtain and process large sample sizes over relatively large geographic areas. In addition, identification of field-collected Culex mosquito specimens to species by morphologic characters is difficult, and verification of species composition in pools often requires use of molecular techniques not commonly available to mosquito surveillance programs. The importance of accurate mosquito species identification is underscored by the indication that Cx. salinarius may have been involved in WN-virus transmission during 1999. This information was not evident from morphologic identification and was determined only by molecular techniques. Accurate identification of species is essential in estimating risk for transmission to humans and directing mosquito control programs.

Acknowledgments

The authors thank S. Aspen, B. Biggerstaff, B. Davis, C. Happ, A. Kerst, K. Volpe, V. Demary, M. Spar, J. Hauer, the staff of the NYC Mayor's Office of Emergency Management, G. Terillion, S. Lindquist, M. Anand, A. Huang, L. McCuiston, and L. Friedlander for their assistance in the field, laboratory, and organizational aspects of this project.

Dr. Nasci is a research entomologist at the Division of Vector-Borne Infectious Diseases infectious diseases: see communicable diseases. , Centers for Disease Control and Prevention, Fort Collins, Colorado. His research interests include the ecology and control of mosquito-transmitted zoonoses Zoonoses

Infections of humans caused by the transmission of disease agents that naturally live in animals. People become infected when they unwittingly intrude into the life cycle of the disease agent and become unnatural hosts.
.

References

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(11.) Hubalek Z, Halouzka J. West Nile fever, a reemerging mosquito-borne viral disease in Europe. Emerg Infect Dis 1999;5:643-50.

(12.) Mitchell CJ, Francy DB, Monath TP. Arthropod arthropod

Any member of the largest phylum, Arthropoda, in the animal kingdom. Arthropoda consists of more than one million known invertebrate species in four subphyla: Uniramia (five classes, including insects), Chelicerata (three classes, including arachnids and horseshoe
 vectors. In: Monath TP, editor. St. Louis encephalitis. Washington: American Public Health Association; 1980. p. 313-79.

(13.) Savage HM, Ceianu C, Nicolescu G, Karabatsos N, Lanciotti R, Vladimirescu LL, et al. Entomologic en·to·mol·o·gy  
n.
The scientific study of insects.



ento·mo·log
 and avian investigations of an epidemic of West Nile fever in Romania in 1996, with serologic se·rol·o·gy  
n. pl. se·rol·o·gies
1. The science that deals with the properties and reactions of serums, especially blood serum.

2.
 and molecular characterization of a virus isolate from mosquitoes. Am J Trop Med Hyg 1999;61:600-11.

(14.) Beaty BJ, Calisher CH, Shope RS. Arboviruses. In: Schimdt NJ, Emmons RW, editors. Diagnostic procedures for viral, rickettsial rickettsial /rick·ett·si·al/ (ri-ket´se-al) pertaining to or caused by rickettsiae.

rick·ett·si·al
adj.
Relating to, or caused by a member of the genus Rickettsia.
 and chlamydial chlamydial

pertaining to members of the family Chlamydiaceae.


chlamydial abortion
abortion in cows, ewes, sows and goat does caused by Chlamydophila abortus and C. pecorum. See enzootic abortion of ewes.
 infections. Washington: American Public Health Association; 1989. p. 797-856.

(15.) Lanciotti RS, Kerst AJ, Nasci RS, Godsey MS, Mitchell CJ, Savage HM, et al. Rapid detection of West Nile virus from human clinical specimens, field collected mosquitoes, and avian samples by a TaqMan RT-PCR assay. J Clin Microbiol 2000;38:4066-71.

(16.) Crabtree MB, Savage HM, Miller BR. Development of a species-diagnostic 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  assay for the identification of Culex vectors of St. Louis encephalitis virus based on interspecies sequence variation in ribosomal DNA spacers. Am J Trop Med Hyg 1995;53:105-9.

(17.) Kokernot RH, Hayes J, Will RL, Radivojevic B, Boyd KR, Chan DHM DHM Deutsches Historisches Museum (Berlin)
DHM Deutsche Harmonia Mundi
DHM Digital Human Modeling
DHM Department of Hydrology and Meteorology (Nepal)
DHM Deep Heat Mining
DHM Diploma in Hotel Management
. Arbovirus studies in the Ohio-Mississippi basin, 1964-1967. III Flanders virus. Am J Trop Med Hyg 1969;18:762-7.

(18.) Calisher CH. Taxonomy, classification, and geographic distribution of California serogroup Bunyaviruses. In: Calisher CH, Thompson WH, editors. California serogroup viruses. New York: Alan R. Liss, Inc.; 1983. p. 1-6.

(19.) Sudia WD, Newhouse VF, Calisher CH, Chamberlain RW. California group arboviruses: isolations from mosquitoes in North America. Mosquito News 1971;31:576-600.

(20.) Mitchell CJ, Francy DB, Monath TP. In: Monath TP, editor. St. Louis encephalitis. Washington: American Public Health Association; 1980. p. 313-79.

(21.) Slaff M, Crans Crans is the name or part of the name of several places:
  • France
  • Crans, Ain, a commune in the Ain département
  • Crans, Jura, a commune in the Jura département
 WJ. Impounded water as a major producer of Culex salinarius (Diptera: Culicidae) in coastal areas of New Jersey, USA. J Med Entomol 1982;19:185-90.

(22.) Pavri KM, Singh KRP KRP Keskusrikospoliisi (Finnish: National Bureau of Investigation)
KRP Karup, Denmark - Karup (Airport Code)
KRP Known Reference Point
KRP Kallang Riverside Park (Singapore) 
. Isolations of West Nile virus from Culex fatigans mosquitoes from western India. Indian J Med Res 1965;53:501-5.

(23.) McIntosh BM, Jupp PG, Dos Santos I, Meenehan GM. Epidemics of West Nile and Sindbis viruses in South Africa with Culex (Culex) univittatus Theobald as vector. S Afr J Sci 1976;72:295-9.

(24.) Bowen GS, Francy DB. Surveillance. In: Monath TP, editor. St. Louis encephalitis. Washington: American Public Health Association; 1980. p. 473-99.

Roger S. Nasci,(*) Dennis J. White,([dagger]) Helen Stirling,([double dagger]) JoAnne Oliver,([dagger]) Thomas J. Daniels,([sections]) Richard C. Falco,([sections]) Scott Campbell,([paragraph]) Wayne J. Crans,(#) Harry M. Savage,(*) Robert S. Lanciotti,(*) Chester G. Moore,(*) Marvin S. Godsey,(*) Kristy L. Gottfried,(*) and Carl J. Mitchell(*)

(*) Centers for Disease Control and Prevention, Fort Collins, Colorado, 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]) New York City Department of Health, New York City, New York, USA; ([sections]) Louis Calder Center The Louis Calder Center is Fordham University's biological field station. The Calder Center is a protected forest preserve located 30 miles north of New York City in Armonk, New York, and is the only full-time ecological research field station in the New York metropolitan area. , Fordham University, Armonk, New York Armonk is a census-designated place (CDP) located in the town of North Castle in Westchester County, New York. As of the 2000 census, the CDP population was 3,461.

Armonk is home to the headquarters of IBM.
, USA; ([paragraph]) Suffolk County Department of Health, Yaphank, New York Yaphank is a hamlet (and census-designated place) in Suffolk County, New York, United States. The population was 5,025 at the 2000 census.

Yaphank is a community in the south part of the Town of Brookhaven.
, USA; and (#) Rutgers University, New Brunswick, New Jersey This article is about the city in New Jersey. For the Canadian province, see New Brunswick.
New Brunswick, also known as "the Healthcare City"[2] or "Hub City",[3] is a city and the county seat of the County of Middlesex, New Jersey, USA.
, USA

Address for correspondence: Roger S. Nasci, CDC-DVBID, P.O. 2087, Fort Collins, CO 80522, USA; fax: 970-221-6476; e-mail: rsn0@cdc.gov
COPYRIGHT 2001 U.S. National Center for Infectious Diseases
No portion of this article can be reproduced without the express written permission from the copyright holder.
Copyright 2001, Gale Group. All rights reserved. Gale Group is a Thomson Corporation Company.

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Author:Mitchell, Carl J.
Publication:Emerging Infectious Diseases
Article Type:Statistical Data Included
Geographic Code:1U2NY
Date:Jul 1, 2001
Words:3829
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