Progress 06/15/05 to 06/14/08
Outputs
OUTPUTS: This special grant provided the basis for bringing together scientists, graduate and undergraduate students, and mosquito abatement and public health personnel. Several topics were studied from different perspectives, particularly the interaction of the mosquito vector and the avian reservoir hosts. In Illinois, a system was devised by which field research funded by the Special Grant, "West Nile Virus, Illinois", was uploaded via Excel spreadsheet to the Illinois Department of Public Health (IDPH), including GIS database information for monitoring West Nile virus activity in mosquitoes, birds, horses, and humans. This consisted of samples from three mosquito abatement districts (MAD) in Cook County (Northwest MAD, North Shore MAD, and DesPlaines River Valley MAD), a mosquito abatement district in Macon County, an intense surveillance program in Champaign and Urbana in central Illinois, and biweekly transects in southern and western Illinois. The results of all field-collected mosquitoes in various research projects that were tested for WNV-RNA were reported to IDPH to be added to the state-wide surveillance by MADs and local health departments. The mosquito samples were tested in the Medical Entomology Laboratory by Real Time-PCR for WNV-RNA, and within 48 hours the results were provided to IDPH (http://www.idph.state.il.us/envhealth/wnv.htm). The results were used by the MAD centers to make decisions on treatment locations, and by IDPH and local public health departments to make risk assessments. From 2005-2007, approximately 30,000 sample sets of mosquitoes were tested, a total of approximately one million individual mosquitoes. Nearly 14% of all sample sets were positive over this time period. As part of this process, infection rates were routinely calculated and supplied to the mosquito abatement groups. The research demonstrated how different testing methods could improve estimation of risk without testing all of the mosquito pools. Email discussions of these results were conducted with the mosquito abatement directors and IDPH personnel. Presentations were made to Audubon Society chapters, University of Illinois entomology students, Green City in the Chicago Department of Environment, and a forum of city commissioners in northern Cook County. Temperature models for mosquito species abundance were placed on the world-wide web. One of the main goals of the output program was to present the results at major conventions related to vector borne diseases, mosquito ecology and behavior, and avian flight behavior and selection by mosquitoes as bloodmeals. Data were also submitted to scientific journals for publication and critical feedback from peers regarding new findings. Oral and poster presentations were made at the American Ornithologist's Union, the Society of Vector Ecologists, American Society of Tropical Medicine and Hygiene, and the American Mosquito Control Association. PARTICIPANTS: The core research group for this project included a principal scientist (Dr. Robert Novak), research scientists (Dr. Richard Lampman and Dr. Weidong Gu), postdoctoral research associates (Dr. Mike Ward and Dr. Osee Sanogo), doctoral collaborators (Dr. Ken Kunkel) and master's level technical scientist (Nina Krasavin). Additional research collaborators included individuals within the Illinois Natural History Survey (Dr. Nohra Mateus) and those from outside academic institutions (see publications). In addition, funds provided summer support for 8 undergraduate students, 8 Master's or Ph.D. level students, and 10 post-baccalaureate students. Undergraduate students, minority students and visiting students from Latin America (Pan American School of Agriculture) were trained. Over the course of this grant, about 30 individuals participated directly in mosquito, avian, virus, and diagnostic research projects. Four individuals conducted their Master's or doctoral research on West Nile virus and an additional four graduate students were funded to do summer work with this program. Several mosquito abatement districts collaborated, sharing their collections to address temporal and spatial questions regarding the distribution of infected mosquito species. These included the directors or field supervisors of Northwest MAD (Mike Szyska), North Shore MAD (Robert Berry), and Des Plaines Valley MAD (Paul Geery) in Cook County and from central Illinois Macon MAD (Robert Millington). Results of all WNV detection tests were provided to the Illinois Department of Public Health with participation by Dr. Linn Haramis, Dr. Curt Colwell, and Ken McCann. Two additional IDPH individuals, Sam Davis and Barb O'Meara, provided assistance in collection of mosquitoes above and below ground in Cook County. They also provided samples for testing from various health departments. Personnel in the environmental section of the local health department in our area, Champaign-Urbana Public Health Department were also collaborators. Presentations at the local meetings provided continuing education credits for IDPH personnel. TARGET AUDIENCES: This special grant brought together researchers and students from different disciplines (entomology, ornithology, climatology, molecular biology, statistical ecology, and landscape ecology) to study the basics aspects of West Nile virus transmission in Illinois. The goals were to define the major vectors and hosts, improve sampling methods for estimation of infection rates and risk, better understand the patterns of interaction between vectors and hosts, and to identify meteorological and biological drivers that regulate the intensity of transmission. The target audiences for these studies include those agencies responsible for vector management (mosquito abatement districts and local public health departments) and disease surveillance (Illinois Department of Public Health and the Centers for Disease Control and Prevention). The data also added to the body of knowledge regarding transmission of arboviruses and the potential risks to members of the general public and other disciplines were explained. Results improved abatement district surveillance systems, as well as provided temporal and spatial estimates of risk (density of infected vectors). Surveillance helped notify the general public about the level of WNV transmission and importance of personal protection measures. Results were shared at various technical society meetings, as well as public forums and with radio, television, and print new media. The results of these efforts helped form a communication network within the state and provided for one of the most widespread collection networks. PROJECT MODIFICATIONS: Nothing significant to report during this reporting period.
Impacts
The effects of WNV on humans and wildlife first became evident when westward movement of the virus extended into the Midwest in 2002, resulting in the first largest arbovirus epidemic in North America and the largest WNV outbreak worldwide. Illinois is relatively unique in the northeastern U.S., enzootic transmission remained high from 2002-2007 and epidemic rebounds occurred in 2005 and 2006. Lower outbreak intensities in other years appeared related to weather. Collaboration with mosquito abatement districts in Cook County revealed spatial and temporal variation in infection rates for Culex mosquitoes. In one study, the proximity of traps to the Des Plaines River Valley Forest Preserve was related to the intensity of transmission (abundance of infected Culex). The forest preserve sites, surrounded by residential and industrial habitats, may act as focal points for bird and mosquito interactions. The prevalence of infected mosquitoes in Cook County was high for extended periods, typically between 5-14% for 3-5 weeks, thus an intense enzootic transmission even in years with low human cases. Stormwater tunnels in the area contained almost exclusively Cx. pipiens during the winter possibly leading to their rapid increase as compared to central Illinois. Some of the spatial variability of infections rates was due to rainfall and landscape factors. A weekly study of infection rates of individual mosquitoes at one site in Cook County suggested the natural competency of Cx. pipiens in the field was less than 50%. Seroprevence studies (by epitope blocking ELISA) and bloodmeal analyses (GenBank sequences) indicated northern cardinals, mourning doves, house sparrows, and American robins were the most commonly infected species. A late season shift in Culex feeding behavior was not observed. Based on research projects throughout the state, there is a 100-fold difference in infection rates in mosquitoes between southern and northern Illinois, but no corresponding stratification in human incidence rates. Bloodmeal analyses are attempting to address whether this is due to geographic variation in the feeding behavior. Molecular methods developed for identification of cryptic Culex species, detected hybrids in the Culex pipiens complex in central Illinois, which is well above the normal hybrid zone. The population trends of 16 urban bird species were estimated before and after the arrival of West Nile virus (WNV) in Illinois and four species showed post-WNV arrival declines (black-capped chickadee, tufted titmouse, blue jay, and American crow) in areas with known high transmission activity.The invasive mosquito species, Aedes (Oc.) japonicus was found in central Illinois and is an active human biter. Studies in central Illinois developed temperature models for predicting Culex pipiens and Cx. restuans abundance (http://mcc.sws.uiuc.edu/research/westnile/background.htm.).
Publications
- Gu, W., Unnasch T. R., 1, Katholib C. R., Lampman, R. and Novak, R.J. 2008. Fundamental issues in mosquito surveillance for arboviral transmission. Trans Royal Soc Trop. Med. Hyg. 102: 817-822.
- Morris, J A.; Lampman, R. L.; Ballmes, G., and Novak, R.J. 2007. First record of Aedes japonicus japonicus in Illinois: Defining its spatial distribution and associated mosquito species. J Am Mosquito Control Assoc. 23:243-251.
- Horn, J. A., M. P. Ward, M. A. Alessi, T. A. Danner, and R. J. Novak. 2007. Observations of a northern cardinal nest reused by a gray catbird in the same season. Wilson Journal of Ornithology 119: 761-763.
- Gu, W., Lampman, R., Krasavin, N., Berry, R. and Novak, R. 2006. Spatio-temporal analysis of West Nile virus transmission in Northern Illinois, 2004. Vector-Borne Zoonotic Diseases 6:91-98.
- Kunkel, K.E., Novak, R.J., Lampman, R. and Gu, W. 2006. Modeling the impact of variable climatic factors on the crossover of Culex restuans and Culex pipiens (Diptera: Culicidae) vectors of West Nile virus in Illinois. Am. J. Trop. Med. Hyg, 74: 168-173.
- Lampman, R.L., Krasavin, N.M., Szyska, M. and Novak, R.J. 2006. A comparison of two West Nile virus detection assays (TaqMan reverse transcriptase-polymerase chain reaction and VecTest antigen assay) during three consecutive outbreaks in northern Illinois. Journal of Am. Mosquito Control Association 22: 76-86.
- Rapaport, A.S., Lampman, R.L. and Novak, R.J. 2006. Evaluation of selected modifications to carbon dioxide and infusion-baited mosquito traps in Urbana, Illinois. J Am Mosquito Control Assoc. 21: 395-399.
- Ward, M.P., Raim, A., Yaremych-Hamer, S., Lampman, R. and Novak, R.J. 2006. Does the roosting behavior of birds affect transmission dynamics of West Nile virus Am. J. Trop. Med. Hyg. 75(2):350-355.
- Sanogo, Y. O., Kim, Chang-Hyun, Lampman, R.L., and Novak R. J. 2008. Identification of male specimens of the Culex pipiens complex (Diptera : Culicidae) in the hybrid zone using morphology and molecular techniques . J. Med. Entomol. 45: 203-209. Sanogo, Y. O., Kim, Chang-Hyun,Lampman, R. L., and Novak R.J. 2007. A real-time TaqMan polymerase chain reaction for the identification of Culex vectors of West Nile and Saint Louis encephalitis viruses in North America. Am. J. Trop. Med. Hyg. 77: 58-66 .
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Progress 06/15/06 to 06/15/07
Outputs
In cooperation with several mosquito abatement districts in Cook Co., IL, approximately 11,000 mosquito pools (nearly 40,000 mosquitoes) were tested for West Nile virus (WNV) in the past year. Nearly 1,800 pools, primarily Culex restuans and Cx. pipiens, were positive. Approximately 400 birds were tested for WNV-antibodies using ELISA, and more than 17% were positive. Infection rates in Culex species collected in Cook County were relatively high over extended periods in 3 of the past 5 years. Prevalence ranged from 4-14% WNV positive for 2-4 weeks of the season. Temperature appeared to be the major regulator of transmission intensity and the increase in infected mosquito pools paralleled the increase in Cx. pipiens abundance. Studies comparing temporal change in vector abundance, infection rate, and human cases by onset date, showed that density of infected mosquitoes was the best indicator of risk to humans, and changes in density tended to precede and parallel
changes in human cases by 2-3 weeks. Spring bird counts and breeding bird surveys throughout Illinois showed declines in populations of corvids and some cavity nesters in areas with high WNV transmission in mosquitoes and humans. Birds contaminated feeders with low levels of WNV. In Cook Co., abundance of Cx. pipiens was greater than in Central Illinois and numbers tended to build up faster in Cook Co., which may reflect higher temperatures in suburban "heat islands" and more underground winter refuges. Recent tests of samples suggest an increase in the discontinuity between VecTests and TaqMan, possibly reflecting local variation in WNV antigenic properties and nucleic acid sequences. Bloodmeal analysis and seroprevalence studies implicated the same avian species as major hosts; American robins, northern cardinals, mourning doves, and house sparrows. The rank in seroprevalence, however, did not necessarily agree with the rank in blood meals. American robins, for example, outnumbered
the other species in the blood meal analysis, but not in seroprevalence. The proportion of mammal vs. bird bloods varied spatially based on abundance of available hosts in the area. Mosquito traps near or in horse stables, cow barns, or pig stables had almost 20% feeding on mammals, whereas blooded mosquitoes caught in residential/campus areas had less than 7% mammal blood. One crow blood and one human blood were found in 50 blood meals identified to species, indicating these species were low preference. In Central Illinois, both molecular analysis and morphology of male reproductive structures showed that hybrids of Cx. pipiens with Cx. quinquefasciatus occur in Champaign-Urbana in August and September. This area is usually considered outside the northern boundary of the hybrid zone. The start of mosquito breeding was early, March and April 2007 in Central Illinois, and early season Cx. restuans were RT-PCR positive. This suggests overwintering Cx. restuans may be the initial source
of enzootic transmission. WNV was not detected in overwintering Cx. pipiens (0 positives out of approx. 3,500 mosquitoes collected from stormwater tunnels).
Impacts
These data challenge several previous conclusions: 1) No late season increase in mammal feeding was found as reported for the East Coast. 2) The blood-feeding pattern must be expressed in terms of both temporal change and spatial availability of hosts; proportion of mammal feedings varies. 3) Decline in WNV transmission tends to begin in early Aug., corresponding to the end of breeding season for common urban mosquito species. 4) Crows are not essential for WNV amplification. 5) Extended collection of egg rafts in Central Illinois when photoperiod is reduced to > 14 hours of light is probably due to the presence of Cx. pipiens complex hybrids that lack an ovarian diapause. A similar late season oviposition pattern was noted for Cook Co, but is unlikely due to Cx. quinquefasciatus hybrids because the location is beyond the hybrid zone. 6) These studies suggest that density of infected mosquitoes is a better indicator of risk than the number of infected biting mosquitoes
x mammal feeding preference x vector competency. 7) These studies provide first evidence that Cx. restuans overwinters the virus in Illinois. 8) Preliminary data suggest the vast underground stormwater/sewage system is responsible for the timing and abundance of Cx. pipiens in Cook Co. These studies established basics of the urban transmission cycle in central and northern IL, and testable hypotheses can now be developed to elucidate critical determinants of transmission and when intervention might be most efficaceous.
Publications
- Lampman, R.L., Slameck, M., Krasavin, N., Kunkel, K. and Novak, R. 2006. Culex population dynamics and West Nile virus transmission in east-central Illinois. Journal American Mosquito Control Assoc. 22(3): 390-400.
- Sanogo, Y.O., Dobson, S.L., Bordenstein, S.R. and Novak, R.J. 2007. Disruption of the Wolbachia surface protein gene wspB by a transposable element in mosquitoes of the Culex pipiens complex (Diptera, Culicidae). Insect Molecular Biology. 16(2):143-154.
- Edillo, F.E. , Kiszewski, A., Hutchinson, M., Bugbee, L., Arias, J., Johnson, J., Gaines, D., Halpaus, J., Cuffee, F., Lampman, R. and Novak, R.J., et al. 2006. ABSTRACT: Population structure of the Culex pipiens vectors of West Nile virus in eastern North America. American Journal of Tropical Medicine and Hygiene 75 (5): 173-173 599 Suppl. S, Nov. 2006.
- Gu, W.D. and Novak, R.J. 2006. Statistical estimation of degree days of mosquito development under fluctuating temperatures in the field. Journal of Vector Ecology. 31(1):107-112.
- Ward, M.P., Raim, A., Yaremych-Hamer, S., Lampman, R. and Novak, R.J. 2006. Does the roosting behavior of birds affect transmission dynamics of West Nile virus? American Journal of Tropical Medicine and Hygiene. 75(2):350-355.
- Bunde, J.M., Heske, E.J., Mateus-Pinilla, N.E., Hofmann, J.E. and Novak, R.J. 2006. A survey for West Nile virus in bats from Illinois. Journal of Wildlife Diseases. 42(2):455-458.
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Progress 06/15/05 to 06/15/06
Outputs
We are comparing seasonal changes in populations of key mosquito species by collecting mosquitoes at selected sites using 5 methods. Multiple sampling methods are used because the efficacy of each method varies by mosquito species, habitat, and physiological state. At each site, mosquitoes are collected for 1-3 days before and during the bird collections in the same area. Collection data are analyzed, in conjunction with meteorological and ecological variables, to determine seasonal trends in regional abundance, indices of mosquito species association, and correlation of key events and temporal events to environmental variables. We are determining abundances of key bird species from northern to southern Illinois from May to September, using surveys in conjunction with bird and mosquito trapping. We are analyzing temporal overlap in host and mosquito abundance and development. Results from the mosquito and host sampling and serology will be added to a statewide
database to help predict disease outbreaks based on samples of hosts and mosquitoes. Sampling and models developed will help estimate the magnitude of the disease, which will be critical for mitigating the incidence of vectors positive for WNV, using appropriate IPM methods in both urban and rural areas, thus helping avert impacts of infection in humans and animals. Sampling of mosquitoes was conducted in 2005 and will continue for the duration of the project. Focused processing of samples by RT-PCR allowed 24-hour turnaround of data and recommendations to mosquito abatement district personnel. Use of RT-PCR as a back-up to the Vec-Test was needed because the Vec-Test kits are adequate for detecting infected mosquitoes, but that approach underestimates recently infected mosquitoes having a low titer of virus. A collaborative study with the Illinois State Water Survey has resulted in a model to predict the rise in Culex pipiens, the main enzootic and suspect epizootic vector of WNV in
Illinois. The prediction for WNV vectors can be found at http://sisyphus.sws.uiuc.edu/research/westnile/index_anim.htm. This model predicts an increasingly early cross-over (50% Cx. pipiens and 50% Cx. restuans abundance in oviposition trap surveys) during warm weather. Cx. pipiens abundance is related to transmission of WNV, which peaks within approximately 2 weeks after cross-over. The long-term project goals are to develop descriptive and quantitative models to predict spatial and temporal interactions of key vector and host populations that influence virus transmission in the state and Midwest.
Impacts
Sampling determines prevalence of West Nile Virus antibodies in different mosquito species as well as in birds, which act as reservoirs for the virus. Our sampling, coupled with the simulation model that we developed, will help managers of mosquito populations understand the incidence of virus infections, allowing them to intervene against mosquitoes in specific areas. Understanding when the cross-over of mosquito species from Cx. restuans to Cx. pipiens occurs allows more-specific management methods to be targeted toward those sites showing the increases in Cx. pipiens.
Publications
- Gu, W. and Novak, R.J. 2005. Habitat-based modeling of impacts of mosquito larval interventions on entomological inoculation rates, incidence and prevalence of malaria. American Journal of Tropical Medicine and Hygiene 73: 546-552.
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Progress 06/15/05 to 06/14/06
Outputs
We examined spatial and temporal distributions of mosquito infection rates and bird seropositive rates in the vicinity of Champaign-Urbana, Illinois. The main West Nile virus (WNV) vectors were Culex pipiens and Culex restuans, outnumbering detections of all other species by 30 to 100 fold. Culex salinarius and Cx. tarsalis (implicated as major vectors in northeast U.S. and west of the Mississippi River, respectively) were present in low abundance and were only rarely positive for WNV. Numbers of Culex pipiens peaked in August and Cx. restuans peaked in July. Degree-day and maximum temperature models (threshold 27C) predicted Cx. pipiens crossover in 2005 to within a day of observed crossover. The largest number of WNV-antibody positive birds were House Sparrows, Northern Cardinals, American Robins, Mourning Doves, and Gray Catbirds. Analysis of Culex specimens was consistent with the avian seropositive rates, verifying the role of Culex and passerine birds as primary
vectors and hosts. Captures of seronegative bird species suggested either low exposure rate or high mortality rate. The temporal patterns of infection rates in mosquitoes and seropositive rates in birds did not parallel each other, except with juvenile birds, reflecting the confounding nature of seasonal bird dispersal patterns and year-to-year survivorship of antibody positive birds. We are sequencing West Nile virus strains collected from different location in Illinois. We also designed DNA probes to discriminate between Culex pipiens, Cx quinquefasciatus, Cx restuans and Cx salinarius, the main WNV vectors in Illinois. We have also developed a real-time PCR technique to detect and quantify West Nile virus vectors, which will help determine the role of each mosquito species in WNV transmission and help target our approach to surveillance and control. In addition to the PCR technique, a new marker derived from Wolbachia bacterium specific to Culex pipiens and Cx. quinquefasciatus was
developed and is being used to study the distribution of the two species in Illinois.
Impacts
These studies help determine which species of mosquitoes are likely vectors of WNV, which helps to target specific control measures. The information on bird infections will aid in assessing morbidity and mortality of Illinois wildlife to WNV, and also to predict which species can serve as bridge vectors of the virus. We showed that the distribution of one vector -- Culex quinquefasciatus -- is expanding north. Moreover, we detected intermediate forms (hybrids) of the two species during the winter. This can have very important health implications because Culex quinquefasciatus -- which bites preferentially mammals including man -- cannot overwinter, whereas Culex pipiens - which feeds mainly on birds -- can overwinter. Their hybrid forms could serve as bridge vector for the transmission of West Nile virus to humans. Using the DNA probes to discriminate between Culex pipiens, Cx quinquefasciatus, Cx restuans and Cx salinarius will help us understand the dynamics of the
main WNV vectors in Illinois. The study is yielding results that will be of value in mosquito management programs, ensuring that infections of humans can be minimized through science-based management recommendations.
Publications
- Gu, W., Lampman, R., Krasavin, N., Berry, R. and Novak, R. 2006. Spatio-temporal analysis of West Nile virus transmission in Northern Illinois, 2004. Vector-Borne Zoonotic Diseases 6:91-98.
- Beveroth, T.A., Ward, M.P., Lampman, R., Ringia, A. and Novak, R.J. 2006. The changes in seroprevalence of West Nile Virus across Illinois in free-ranging birds from 2001-2004. American Journal of Tropical Medicine and Hygiene 74: 174-179.
- Novak, R.J. and Gerberg, E.J. 2006. Natural-based repellent products: Efficacy for military and general public uses. J. American Mosquito Control Assoc., Supplement, current trends in repellent technology 21: 7-12.
- Davis, C.T., Ebel, G.D., Lanciotti, R.S., Brault, A.C., Guzman, H., Siirin, M., Parsons, R.E., Beasley, D.W.C., Novak, R.J., Elizondo-Quiroga, D., Green, E.N., Young, D.S., Stark, L.M., Artsob, H., Tesh, R.B., Kramer, L.D. and Barrett, A.D.T. 2005. Phylogenetic analysis of North American West Nile virus isolates 2001-2004: Evidence for the emergence of a dominant genotype. Virology 342: 252-265.
- Reno, H. and Novak, R.J. 2005. Characterization of a pyrase-like activity in Aedes triseriatus, Aedes hendersoni and Aedes aegypti. American Journal of Tropical Medicine and Hygiene 73: 541-545.
- Jacob, B., Nelson, P.G., Lampman, R., Morris, J., Raim, A., Funes, J., LaPointe, C. and Novak, R. 2005. Comparing GPS technology for identifying spatial ecological variation for urban mosquito management. Wing Beats 16: 30-33.
- Rapaport, A.S., Lampman, R.L. and Novak, R.J. 2006. Evaluation of selected modifications to carbon dioxide and infusion-baited mosquito traps in Urbana, Illinois. Journal American Mosquito Control Association 21: 395-399.
- Kunkel, K.E., Novak, R.J., Lampman, R. and Gu, W.. 2006. Modeling the impact of variable climatic factors on the crossover of Culex restuans and Culex pipiens (Diptera: Culicidae) vectors of West Nile virus in Illinois. American Journal of Tropical Medicine and Hygiene 74: 168-173.
- Lampman, R.L., Krasavin, N.M., Szyska, M. and Novak, R.J. 2006. A comparison of two West Nile virus detection assays (TaqMan reverse transcriptase-polymerase chain reaction and VecTest antigen assay) during three consecutive outbreaks in northern Illinois. Journal of Am. Mosquito Control Association 22: 76-86.
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