Scott R. Campbell

West Nile Virus Risk Assessment and the Bridge Vector Paradigm

In the northeast United States, control of West Nile virus (WNV) vectors has been unfocused because of a lack of accurate knowledge about the roles different mosquitoes play in WNV transmission. We analyzed the risk posed by 10 species of mosquitoes for transmitting WNV to humans by using a novel risk-assessment measure that combines information on the abundance, infection prevalence, vector competence, and biting behavior of vectors. This analysis suggests that 2 species (Culex pipiens L. and Cx. restuans Theobald [Diptera: Cilicidae]) not previously considered important in transmitting WNV to humans may be responsible for up to 80% of human WNV infections in this region. This finding suggests that control efforts should be focused on these species which may reduce effects on nontarget wetland organisms. Our risk measure has broad applicability to other regions and diseases and can be adapted for use as a predictive tool of future human WNV infections.

Prevalence of Ehrlichia, Borrelia, and Rickettsial agents in Amblyomma americanum (Acari: Ixodidae) collected from nine states.

Abstract Ambyomma americanum (L.) (Acari: Ixodidae) is an aggressive tick that feeds on humans during all postembryonic life stages. In many regions of the United States, it is the tick most commonly found attached to humans. Public health interest has grown recently, due to the recognition of new human pathogens transmitted by A. americanum and the expanding distribution of the tick. A. americanum is a vector of several bacteria pathogenic to humans. Ehrlichia chaffeensis and Ehrlichia ewingii cause moderate-to-severe febrile illness. “Rickettsia amblyommii,” a member of the spotted fever group Rickettsia, also has recently been implicated as a possible human pathogen based on serologic evidence from persons recovering from illness after a tick bite. We have determined the prevalence of infection of Ehrlichia chaffeensis, E. ewingii, “Borrelia lonestari,” and R. amblyommii within A. americanum ticks from 29 sites in nine states. Overall infection prevalences were 4.7% for E. chaffeensis (range, 0–27%), 3.5% for E. ewingii (range, 0–18.6%), 2.5% for B. lonestari (range, 0–12.2%), and 41.2% for R. amblyommii (range, 0–84.0%). In addition, 87 ticks (4.3%) were infected with two or more bacteria. This report documents new distribution records for E. ewingii, B. lonestari, and R. amblyommii and underscores the nonhomogeneous distribution of pathogen foci of infection. Additional surveillance throughout the range of A. americanum is warranted to increase physician and public awareness of the risk of disease to humans from exposure to the agents transmitted by this tick.

Aedes (Finlaya) japonicus (Diptera: Culicidae), a Newly Recognized Mosquito in the United States: Analyses of Genetic Variation in the United States and Putative Source Populations

Abstract Introduction of potential disease vectors into a new geographic area poses health risks to local human, livestock, and wildlife populations. It is therefore important to gain understanding of the dynamics of these invasions, in particular its sources, modes of spread after the introduction, and vectorial potential. We studied the population genetics of Aedes (Finlaya) japonicus japonicus (Theobald), an Asian mosquito that was recognized for the first time in the United States in 1998. We examined patterns of genetic diversity using random amplified polymorphic DNA and sequences of ND4 of mtDNA by comparing samples from populations spanning the range of this mosquito in Japan (six samples) and the United States (nine samples) as well as specimens intercepted in New Zealand in 1999. We found geographically differentiated populations in Japan, indicating limited gene flow even on small spatial scales. In the United States, we found evidence of significant genetic differentiation between samples from New York, Connecticut, and New Jersey and those from mid-Pennsylvania and Maryland. We were unable to pinpoint the source location(s) in Japan, although some of the U.S. samples are genetically close to samples from south Honshu and western Kyushu. Further studies should include samples from Korean populations. Distinct genetic signatures in U.S. populations undergoing expansion suggest the possibility of local increases in genetic diversity if and where they meet.

Genotypic Variation and Mixtures of Lyme Borrelia in Ixodes Ticks from North America and Europe

Background Lyme disease, caused by various species of Borrelia, is transmitted by Ixodes ticks in North America and Europe. Studies have shown the genotype of Borrelia burgdorferi sensu stricto (s.s.) or the species of B. burgdorferi sensu lato (s.l.) affects the ability of the bacteria to cause local or disseminated infection in humans. Methodology/Principal Findings We used a multilocus PCR electrospray mass spectrometry assay to determine the species and genotype Borrelia from ticks collected in New York, Connecticut, Indiana, Southern Germany, and California and characterized isolates from parts of the United States and Europe. These analyses identified 53 distinct genotypes of B. burgdorferi sensu stricto with higher resolution than ospC typing. Genotypes of other members of the B. burgdorferi sensu lato complex were also identified and genotyped including B. afzelii, B. garinii, B. lusitaniae, B. spielmanii, and B. valaisiana. While each site in North America had genotypes unique to that location, we found genotypes shared between individual regions and two genotypes found across the United States. Significant B. burgdorferi s.s. genotypic diversity was observed between North America and Europe: only 6.6% of US genotypes (3 of 45) were found in Europe and 27% of the European genotypes (3 of 11) were observed in the US. Interestingly, 39% of adult Ixodes scapularis ticks from North America were infected with more than one genotype of B. burgdorferi s.s. and 22.2% of Ixodes ricinus ticks from Germany were infected with more than one genotype of B. burgdorferi s.l. Conclusions/Significance The presence of multiple Borrelia genotypes in ticks increases the probability that a person will be infected with more than one genotype of B. burgdorferi, potentially increasing the risks of disseminated Lyme disease. Our study indicates that the genotypic diversity of Borrelia in ticks in both North America and Europe is higher then previously reported and can have potential clinical consequences.

Predictive Mapping of Human Risk for West Nile Virus (WNV) Based on Environmental and Socioeconomic Factors

A West Nile virus (WNV) human risk map was developed for Suffolk County, New York utilizing a case-control approach to explore the association between the risk of vector-borne WNV and habitat, landscape, virus activity, and socioeconomic variables derived from publically available datasets. Results of logistic regression modeling for the time period between 2000 and 2004 revealed that higher proportion of population with college education, increased habitat fragmentation, and proximity to WNV positive mosquito pools were strongly associated with WNV human risk. Similar to previous investigations from north-central US, this study identified middle class suburban neighborhoods as the areas with the highest WNV human risk. These results contrast with similar studies from the southern and western US, where the highest WNV risk was associated with low income areas. This discrepancy may be due to regional differences in vector ecology, urban environment, or human behavior. Geographic Information Systems (GIS) analytical tools were used to integrate the risk factors in the 2000–2004 logistic regression model generating WNV human risk map. In 2005–2010, 41 out of 46 (89%) of WNV human cases occurred either inside of (30 cases) or in close proximity (11 cases) to the WNV high risk areas predicted by the 2000–2004 model. The novel approach employed by this study may be implemented by other municipal, local, or state public health agencies to improve geographic risk estimates for vector-borne diseases based on a small number of acute human cases.

Comparative Analysis of Distribution and Abundance of West Nile and Eastern Equine Encephalomyelitis Virus Vectors in Suffolk County, New York, Using Human Population Density and Land Use/Cover Data

Abstract Five years of CDC light trap data from Suffolk County, NY, were analyzed to compare the applicability of human population density (HPD) and land use/cover (LUC) classification systems to describe mosquito abundance and to determine whether certain mosquito species of medical importance tend to be more common in urban (defined by HPD) or residential (defined by LUC) areas. Eleven study sites were categorized as urban or rural using U.S. Census Bureau data and by LUC types using geographic information systems (GISs). Abundance and percent composition of nine mosquito taxa, all known or potential vectors of arboviruses, were analyzed to determine spatial patterns. By HPD definitions, three mosquito species, Aedes canadensis (Theobald), Coquillettidia perturbans (Walker), and Culiseta melanura (Coquillett), differed significantly between habitat types, with higher abundance and percent composition in rural areas. Abundance and percent composition of these three species also increased with freshwater wetland, natural vegetation areas, or a combination when using LUC definitions. Additionally, two species, Ae. canadensis and Cs. melanura, were negatively affected by increased residential area. One species, Aedes vexans (Meigen), had higher percent composition in urban areas. Two medically important taxa, Culex spp. and Aedes triseriatus (Say), were proportionally more prevalent in residential areas by LUC classification, as was Aedes trivittatus (Coquillett). Although HPD classification was readily available and had some predictive value, LUC classification resulted in higher spatial resolution and better ability to develop location specific predictive models.

Assays to Detect West Nile Virus in Dead Birds

Using oral swab samples to detect West Nile virus in dead birds, we compared the Rapid Analyte Measurement Platform (RAMP) assay with VecTest and real-time reverse-transcriptase–polymerase chain reaction. The sensitivities of RAMP and VecTest for testing corvid species were 91.0% and 82.1%, respectively.

Detection of Ehrlichia chaffeensis in Adult and Nymphal Amblyomma americanum (Acari: Ixodidae) Ticks from Long Island, New York

Abstract The lone star tick, Amblyomma americanum (L.), has increased in abundance in several regions of the northeastern United States, including areas of Long Island, NY. Adult and nymphal stage A. americanum collected from several sites on Long Island were evaluated for infection with Ehrlichia chaffeensis, the causative agent of human monocytic ehrlichiosis (HME), by using a nested polymerase chain reaction assay. Fifty-nine (12.5%) of 473 adults and eight of 113 pools of five nymphs each (estimated minimum prevalence of infection 1.4%) contained DNA of E. chaffeensis. These data, coupled with the documented expansion of lone star tick populations in the northeastern United States, confirm that E. chaffeensis is endemic to many areas of Long Island and that HME should be considered among the differential diagnoses of the many distinct tick-borne diseases that occur in this region.

Meteorological and Hydrological Influences on the Spatial and Temporal Prevalence of West Nile Virus in Culex Mosquitoes, Suffolk County, New York

ABSTRACT The factors determining the spatial and temporal distribution of West Nile virus (family Flaviviridae, genus Flavivirus, WNV) activity are not well understood. Here, we explore the effects of hydrological and meteorological conditions on WNV infection among Culex genus mosquitoes collected during 2001–2009 in Suffolk County, Long Island, NY. We show that WNV infection rates in assayed pools of Culex mosquitoes are associated in both space and time with hydrological and meteorological variability. Specifically, wet winter, warm and wet spring conditions, and dry summer conditions are associated with the increased local prevalence of WNV among Culex mosquitoes during summer and fall. These findings indicate that within Suffolk County, and for a given year, areas at risk for heightened WNV activity may be identified in advance by using hydrology model estimates of land surface wetness and observed meteorological conditions.

SALT MARSH AS CULEX SALINARIUS LARVAL HABITAT IN COASTAL NEW YORK

ABSTRACT Culex salinarius is considered one of the most likely bridge vectors involved in the human transmission cycle of West Nile virus (WNV) and eastern equine encephalomyelitis virus (EEEV) in the northeastern USA. The larval habitats of this species in the coastal region of New York State are currently poorly known. Between 2005 and 2007, a larval survey was carried out to identify and characterize possible larval habitats in Suffolk County, encompassing natural and man-made freshwater wetlands, artificial containers, and salt marshes. Only relatively undisturbed salt marsh yielded Cx. salinarius larvae in considerable numbers from several sites over a period of 2 years. The immature stages of this species were found associated with Spartina patens and S. alterniflora of the upper marsh at salinities ranging from 4.3 to 18.8 parts per thousand. Both heavily impacted and relatively undisturbed salt marshes produced several hundreds of adult Cx. salinarius per Centers for Disease Control and Prevention (CDC) light trap per night, an order of magnitude higher than CDC light traps deployed at upland sites. The ability of Cx. salinarius to use both heavily impacted and relatively undisturbed salt marshes for reproduction has significant repercussions for marsh restoration and vector control practices.