Chester G. Moore

The global distribution of the arbovirus vectors Aedes aegypti and Ae. albopictus

Dengue and chikungunya are increasing global public health concerns due to their rapid geographical spread and increasing disease burden. Knowledge of the contemporary distribution of their shared vectors, Aedes aegypti and Aedes albopictus remains incomplete and is complicated by an ongoing range expansion fuelled by increased global trade and travel. Mapping the global distribution of these vectors and the geographical determinants of their ranges is essential for public health planning. Here we compile the largest contemporary database for both species and pair it with relevant environmental variables predicting their global distribution. We show Aedes distributions to be the widest ever recorded; now extensive in all continents, including North America and Europe. These maps will help define the spatial limits of current autochthonous transmission of dengue and chikungunya viruses. It is only with this kind of rigorous entomological baseline that we can hope to project future health impacts of these viruses. DOI: http://dx.doi.org/10.7554/eLife.08347.001

The global compendium of Aedes aegypti and Ae. albopictus occurrence.

Aedes aegypti and Ae. albopictus are the main vectors transmitting dengue and chikungunya viruses. Despite being pathogens of global public health importance, knowledge of their vectors’ global distribution remains patchy and sparse. A global geographic database of known occurrences of Ae. aegypti and Ae. albopictus between 1960 and 2014 was compiled. Herein we present the database, which comprises occurrence data linked to point or polygon locations, derived from peer-reviewed literature and unpublished studies including national entomological surveys and expert networks. We describe all data collection processes, as well as geo-positioning methods, database management and quality-control procedures. This is the first comprehensive global database of Ae. aegypti and Ae. albopictus occurrence, consisting of 19,930 and 22,137 geo-positioned occurrence records respectively. Both datasets can be used for a variety of mapping and spatial analyses of the vectors and, by inference, the diseases they transmit.

Transmission dynamics of an insect-specific flavivirus in a naturally infected Culex pipiens laboratory colony and effects of co-infection on vector competence for West Nile virus.

We established a laboratory colony of Culex pipiens mosquitoes from eggs collected in Colorado and discovered that mosquitoes in the colony are naturally infected with Culex flavivirus (CxFV), an insect-specific flavivirus. In this study we examined transmission dynamics of CxFV and effects of persistent CxFV infection on vector competence for West Nile virus (WNV). We found that vertical transmission is the primary mechanism for persistence of CxFV in Cx. pipiens, with venereal transmission potentially playing a minor role. Vector competence experiments indicated possible early suppression of WNV replication by persistent CxFV infection in Cx. pipiens. This is the first description of insect-specific flavivirus transmission dynamics in a naturally infected mosquito colony and the observation of delayed dissemination of superinfecting WNV suggests that the presence of CxFV may impact the intensity of enzootic transmission of WNV and the risk of human exposure to this important pathogen.

Use of Google Earth to strengthen public health capacity and facilitate management of vector-borne diseases in resource-poor environments.

OBJECTIVE Novel, inexpensive solutions are needed for improved management of vector-borne and other diseases in resource-poor environments. Emerging free software providing access to satellite imagery and simple editing tools (e.g. Google Earth) complement existing geographic information system (GIS) software and provide new opportunities for: (i) strengthening overall public health capacity through development of information for city infrastructures; and (ii) display of public health data directly on an image of the physical environment. METHODS We used freely accessible satellite imagery and a set of feature-making tools included in the software (allowing for production of polygons, lines and points) to generate information for city infrastructure and to display disease data in a dengue decision support system (DDSS) framework. FINDINGS Two cities in Mexico (Chetumal and Merida) were used to demonstrate that a basic representation of city infrastructure useful as a spatial backbone in a DDSS can be rapidly developed at minimal cost. Data layers generated included labelled polygons representing city blocks, lines representing streets, and points showing the locations of schools and health clinics. City blocks were colour-coded to show presence of dengue cases. The data layers were successfully imported in a format known as shapefile into a GIS software. CONCLUSION The combination of Google Earth and free GIS software (e.g. HealthMapper, developed by WHO, and SIGEpi, developed by PAHO) has tremendous potential to strengthen overall public health capacity and facilitate decision support system approaches to prevention and control of vector-borne diseases in resource-poor environments.

Insect-Specific Flaviviruses from Culex Mosquitoes in Colorado, with Evidence of Vertical Transmission

Mosquitoes were collected in Colorado during 2006 and 2007 to examine spatial and seasonal patterns of risk for exposure to Culex vectors and West Nile virus. We used universal flavivirus primers to test pools of Culex mosquitoes for viral RNA. This led to the detection and subsequent isolation of two insect-specific flaviviruses: Culex flavivirus (CxFV), which was first described from Japan, and a novel insect flavivirus, designated Calbertado virus (CLBOV), which has also been detected in California and Canada. We recorded both viruses in Cx. tarsalis and Cx. pipiens from Colorado. Furthermore, quantitative reverse transcription polymerase chain reaction (RT-PCR) revealed the presence of CxFV RNA in Cx. pipiens eggs and larvae from a laboratory colony established in 2005 and naturally infected with CxFV, suggesting vertical transmission as a means of viral maintenance in natural Culex populations. Finally, we present phylogenetic analyses of the relationships between insect-specific flaviviruses and other selected flaviviruses.

Aedes (Stegomyia) aegypti in the Continental United States: A Vector at the Cool Margin of Its Geographic Range

ABSTRACT After more than a half century without recognized local dengue outbreaks in the continental United States, there were recent outbreaks of autochthonous dengue in the southern parts of Texas (2004–2005) and Florida (2009–2011). This dengue reemergence has provoked interest in the extent of the future threat posed by the yellow fever mosquito, Aedes (Stegomyia) aegypti (L.), the primary vector of dengue and yellow fever viruses in urban settings, to human health in the continental United States. Ae. aegypti is an intriguing example of a vector species that not only occurs in the southernmost portions of the eastern United States today but also is incriminated as the likely primary vector in historical outbreaks of yellow fever as far north as New York, Philadelphia, and Boston, from the 1690s to the 1820s. For vector species with geographic ranges limited, in part, by low temperature and cool range margins occurring in the southern part of the continental United States, as is currently the case for Ae. aegypti, it is tempting to speculate that climate warming may result in a northward range expansion (similar to that seen for Ixodes tick vectors of Lyme borreliosis spirochetes in Scandinavia and southern Canada in recent decades). Although there is no doubt that climate conditions directly impact many aspects of the life history of Ae. aegypti, this mosquito also is closely linked to the human environment and directly influenced by the availability of water-holding containers for oviposition and larval development. Competition with other container-inhabiting mosquito species, particularly Aedes (Stegomyia) albopictus (Skuse), also may impact the presence and local abundance of Ae. aegypti. Field-based studies that focus solely on the impact of weather or climate factors on the presence and abundance of Ae. aegypti, including assessments of the potential impact of climate warming on the mosquitos future range and abundance, do not consider the potential confounding effects of socioeconomic factors or biological competitors for establishment and proliferation of Ae. aegypti. The results of such studies therefore should not be assumed to apply in areas with different socioeconomic conditions or composition of container-inhabiting mosquito species. For example, results from field-based studies at the high altitude cool margins for Ae. aegypti in Mexicos central highlands or the Andes in South America cannot be assumed to be directly applicable to geographic areas in the United States with comparable climate conditions. Unfortunately, we have a very poor understanding of how climatic drivers interact with the human landscape and biological competitors to impact establishment and proliferation of Ae. aegypti at the cool margin of its range in the continental United States. A first step toward assessing the future threat this mosquito poses to human health in the continental United States is to design and conduct studies across strategic climatic and socioeconomic gradients in the United States (including the U.S.-Mexico border area) to determine the permissiveness of the coupled natural and human environment for Ae. aegypti at the present time. This approach will require experimental studies and field surveys that focus specifically on climate conditions relevant to the continental United States. These studies also must include assessments of how the human landscape, particularly the impact of availability of larval developmental sites and the permissiveness of homes for mosquito intrusion, and the presence of other container-inhabiting mosquitoes that may compete with Ae. aegypti for larval habitat affects the ability of Ae. aegypti to establish and proliferate. Until we are armed with such knowledge, it is not possible to meaningfully assess the potential for climate warming to impact the proliferation potential for Ae. aegypti in the United States outside of the geographic areas where the mosquito already is firmly established, and even less so for dengue virus transmission and dengue disease in humans.

Entomological studies along the Colorado front range during a period of intense west nile virus activity

ABSTRACT To better understand the ecology of West Nile virus transmission in Northern Colorado, field studies were conducted in Larimer and Weld counties from September 2003 through March 2005. During summer studies, 18,540 adult mosquitoes were collected using light traps and gravid traps. West Nile virus RNA was detected in 24 of the 2,140 mosquito pools tested throughout the study area in 2003 and 2004. Culex tarsalis had the highest minimum infection rate (MIR) in both 2003 (MIR  =  34.48) and in 2004 (MIR  =  8.74). During winter studies, 9,391 adult mosquitoes were collected by aspirator from various overwintering sites including bridges and storm drains. The most frequently collected species was Culex pipiens. West Nile virus was not detected in our overwintering collections. The relationship between spring adult emergence and temperature inside and outside overwintering sites is described. Species composition of collections as well as the spatial and temporal distribution of West Nile virus detections are presented.

Seasonal Patterns for Entomological Measures of Risk for Exposure to Culex Vectors and West Nile Virus in Relation to Human Disease Cases in Northeastern Colorado

ABSTRACT We examined seasonal patterns for entomological measures of risk for exposure to Culex vectors and West Nile virus (family Flaviviridae, genus Flavivirus, WNV) in relation to human WNV disease cases in a five-county area of northeastern Colorado during 2006–2007. Studies along habitat/ elevation gradients in 2006 showed that the seasonal activity period is shortened and peak numbers occur later in the summer for Culex tarsalis Coquillett females in foothills-montane areas > 1,600 m compared with plains areas <1,600 m in Colorados Front Range. Studies in the plains of northeastern Colorado in 2007 showed that seasonal patterns of abundance for Cx. tarsalis and Culex pipiens L. females differed in that Cx. tarsalis reached peak abundance in early July (mean of 328.9 females per trap night for 18 plains sites), whereas the peak for Cx. pipiens did not occur until late August (mean of 16.4 females per trap night). During June-September in 2007, which was a year of intense WNV activity in Colorado with 578 reported WNV disease cases, we recorded WNV-infected Cx. tarsalis females from 16 of 18 sites in the plains. WNV infection rates in Cx. tarsalis females increased gradually from late June to peak in mid-August (overall maximum likelihood estimate for WNV infection rate of 8.29 per 1,000 females for the plains sites in mid-August). No WNV-infected Culex mosquitoes were recorded from sites > 1,600 m. The vector index for abundance of WNV-infected Cx. tarsalis females for the plains sites combined exceeded 0.50 from mid-July to mid-August, with at least one site exceeding 1.00 from early July to late August. Finally, we found that abundance of Cx. tarsalis females and the vector index for infected females were strongly associated with weekly numbers of WNV disease cases with onset 4–7 wk later (female abundance) or 1–2 wk later (vector index).

Mosquito Species Richness, Composition, and Abundance along Habitat-Climate-Elevation Gradients in the Northern Colorado Front Range

Abstract We exploited elevation gradients (1,500–2,400 m) ranging from plains to montane areas along the Poudre River and Big Thompson River in the northern Colorado Front Range to determine how mosquito species richness, composition, and abundance change along natural habitat-climate-elevation gradients. Mosquito collections in 26 sites in 2006 by using CO2-baited CDC light traps yielded a total of 7,136 identifiable mosquitoes of 27 species. Commonly collected species included Aedes vexans (Meigen) (n = 4,722), Culex tarsalis Coquillett (n = 825), Ochlerotatus increpitus (Dyar) (n = 546), Ochlerotatus trivittatus (Coquillett) (n = 303), Aedes cinereus Meigen (n = 280), Ochlerotatus melanimon (Dyar) (n = 146), Ochlerotatus dorsalis (Meigen) (n = 67), Culiseta inornata (Williston) (n = 52), Ochlerotatus pullatus (Coquillett) (n = 38), Ochlerotatus spencerii idahoensis (Theobald) (n = 37), and Culex pipiens L. (n = 29). Species richness was highest in plains habitats at elevations below 1,600 m. Numerous species were found exclusively or predominantly at low elevations below 1,700 m [Anopheles earlei Vargas, Anopheles freeborni Aitken, Coquilletidia perturbans (Walker), Culex erythrothorax (Dyar), Cx. pipiens, Culex territans Walker, Oc. dorsalis, Ochlerotatus hendersoni (Cockerell), Oc. melanimon, and Oc. trivittatus], whereas others occurred predominantly at high elevations above 2,300 m [Ae. cinereus, Culiseta incidens (Thomson), Culiseta morsitans (Theoblad), Ochlerotatus cataphylla (Dyar), Ochlerotatus intrudens (Dyar), Oc. pullatus, and Ochlerotatus punctor (Kirby)]. Ae. vexans and Cx. tarsalis were abundant in the plains (<1,600 m; mean June–August temperature >19.5°C), occurred at low abundances in foothills and low montane areas (1,610–1,730 m; 18.0–19.5°C), and they were collected only sporadically in montane areas above 1,750 m (mean June–August temperature <17.5°C). These findings suggest that future climate warming may lead to shifts in distribution patterns of West Nile virus vectors (e.g., Cx. tarsalis) toward higher elevations in Colorado.

Mosquitoes and West Nile virus along a river corridor from prairie to montane habitats in eastern Colorado

ABSTRACT: We conducted studies on mosquitoes and West Nile virus (WNV) along a riparian corridor following the South Platte River and Big Thompson River in northeastern Colorado and extending from an elevation of 1,215 m in the prairie landscape of the eastern Colorado plains to 1,840 m in low montane areas at the eastern edge of the Rocky Mountains in the central part of the state. Mosquito collection during June–September 2007 in 20 sites along this riparian corridor yielded a total of 199,833 identifiable mosquitoes of 17 species. The most commonly collected mosquitoes were, in descending order: Aedes vexans, Culex tarsalis, Ae. dorsalis, Ae. trivittatus, Ae. melanimon, Cx. pipiens, and Culiseta inornata. Species richness was higher in the plains than in foothills-montane areas, and abundances of several individual species, including the WNV vectors Cx. tarsalis and Cx. pipiens and the nuisance-biter and potential secondary WNV vector Ae. vexans, decreased dramatically from the plains (1,215–1,487 m) to foothills-montane areas (1,524–1,840 m). Ae. vexans and Cx. tarsalis had a striking pattern of uniformly high abundances between 1,200–1,450 m followed by a gradual decrease in abundance above 1,450 m to reach very low numbers above 1,550 m. Culex species were commonly infected with WNV in the plains portion of the riparian corridor in 2007, with 14 of 16 sites yielding WNV-infected Cx. tarsalis and infection rates for Cx. tarsalis females exceeding 2.0 per 1,000 individuals in ten of the sites. The Vector Index for abundance of WNV-infected Cx. tarsalis females during June–September exceeded 0.5 in six plains sites along the South Platte River but was uniformly low (0–0.1) in plains, foothills and montane sites above 1,500 m along the Big Thompson River. A population genetic analysis of Cx. tarsalis revealed that all collections from the ∼190 km riparian transect in northeastern Colorado were genetically uniform but that these collections were genetically distinct from collections from Delta County on the western slope of the Continental Divide. This suggests that major waterways in the Great Plains serve as important dispersal corridors for Cx. tarsalis but that the Continental Divide is a formidable barrier to this WNV vector.