Penny Masuoka

The AFHSC-Division of GEIS Operations Predictive Surveillance Program: a multidisciplinary approach for the early detection and response to disease outbreaks

The Armed Forces Health Surveillance Center, Division of Global Emerging Infections Surveillance and Response System Operations (AFHSC-GEIS) initiated a coordinated, multidisciplinary program to link data sets and information derived from eco-climatic remote sensing activities, ecologic niche modeling, arthropod vector, animal disease-host/reservoir, and human disease surveillance for febrile illnesses, into a predictive surveillance program that generates advisories and alerts on emerging infectious disease outbreaks. The program’s ultimate goal is pro-active public health practice through pre-event preparedness, prevention and control, and response decision-making and prioritization. This multidisciplinary program is rooted in over 10 years experience in predictive surveillance for Rift Valley fever outbreaks in Eastern Africa. The AFHSC-GEIS Rift Valley fever project is based on the identification and use of disease-emergence critical detection points as reliable signals for increased outbreak risk. The AFHSC-GEIS predictive surveillance program has formalized the Rift Valley fever project into a structured template for extending predictive surveillance capability to other Department of Defense (DoD)-priority vector- and water-borne, and zoonotic diseases and geographic areas. These include leishmaniasis, malaria, and Crimea-Congo and other viral hemorrhagic fevers in Central Asia and Africa, dengue fever in Asia and the Americas, Japanese encephalitis (JE) and chikungunya fever in Asia, and rickettsial and other tick-borne infections in the U.S., Africa and Asia.

Ecological niche model of Phlebotomus alexandri and P. papatasi (Diptera: Psychodidae) in the Middle East

BackgroundThe purpose of this study is to create distribution models of two sand fly species, Phlebotomus papatasi (Scopoli) and P. alexandri (Sinton), across the Middle East. Phlebotomus alexandri is a vector of visceral leishmaniasis, while P. papatasi is a vector of cutaneous leishmaniasis and sand fly fever. Collection records were obtained from literature reports from 1950 through 2007 and unpublished field collection records. Environmental layers considered in the model were elevation, precipitation, land cover, and WorldClim bioclimatic variables. Models were evaluated using the threshold-independent area under the curve (AUC) receiver operating characteristic analysis and the threshold-dependent minimum training presence.ResultsFor both species, land cover was the most influential environmental layer in model development. The bioclimatic and elevation variables all contributed to model development; however, none influenced the model as strongly as land cover.ConclusionWhile not perfect representations of the absolute distribution of P. papatasi and P. alexandri, these models indicate areas with a higher probability of presence of these species. This information could be used to help guide future research efforts into the ecology of these species and epidemiology of the pathogens that they transmit.

Ecological niche modeling to estimate the distribution of Japanese encephalitis virus in Asia.

Background Culex tritaeniorhynchus is the primary vector of Japanese encephalitis virus (JEV), a leading cause of encephalitis in Asia. JEV is transmitted in an enzootic cycle involving large wading birds as the reservoirs and swine as amplifying hosts. The development of a JEV vaccine reduced the number of JE cases in regions with comprehensive childhood vaccination programs, such as in Japan and the Republic of Korea. However, the lack of vaccine programs or insufficient coverage of populations in other endemic countries leaves many people susceptible to JEV. The aim of this study was to predict the distribution of Culex tritaeniorhynchus using ecological niche modeling. Methods/Principal Findings An ecological niche model was constructed using the Maxent program to map the areas with suitable environmental conditions for the Cx. tritaeniorhynchus vector. Program input consisted of environmental data (temperature, elevation, rainfall) and known locations of vector presence resulting from an extensive literature search and records from MosquitoMap. The statistically significant Maxent model of the estimated probability of Cx. tritaeniorhynchus presence showed that the mean temperatures of the wettest quarter had the greatest impact on the model. Further, the majority of human Japanese encephalitis (JE) cases were located in regions with higher estimated probability of Cx. tritaeniorhynchus presence. Conclusions/Significance Our ecological niche model of the estimated probability of Cx. tritaeniorhynchus presence provides a framework for better allocation of vector control resources, particularly in locations where JEV vaccinations are unavailable. Furthermore, this model provides estimates of vector probability that could improve vector surveillance programs and JE control efforts.

Spatial correlations of mapped malaria rates with environmental factors in Belize, Central America

BackgroundThe purposes of this study were to map overall malaria incidence rates from 1989 through 1999 for villages in Belize; to assess the seasonal distribution of malaria incidence by region; and to correlate malaria incidence rates with vegetation cover and rivers in villages, using geographic information system technology.Malaria information on 156 villages was obtained from an electronic database maintained by the Belize National Malaria Control Program. Average annual malaria incidence rates per 1000 population over 10 years were calculated for villages using the 1991 population census as a denominator. Malaria incidence rates were integrated with vegetation cover from a 1995 vegetation map, and with river data from a digital data set.ResultsMapping malaria incidence over the 10-year period in the study villages indicated the existence of a spatial pattern: the southern and western areas of Belize had consistently higher rates of malaria than northern areas. Examination of the seasonal distribution of malaria incidence by month over 10 years indicated that a statistically significant difference existed among districts and among months (p < 0.05). Spatial analysis of malaria incidence rates and of vegetation in Belize showed villages with high malaria rates having more broadleaf hill forests, agricultural land, and wetland vegetation types (i.e. SWF-seasonally waterlogged fire-induced shrubland of the plains). Statistical and spatial analyses of malaria incidence and of river distributions in Belize determined the high 10 percentile malaria incidence villages in western and southern Belize to have more rivers within two kilometers of the center of a village and a statistically significant correlation between proximity to rivers and villages (Spearmans γ = -0.23; p < 0.05), especially in Stann Creek District (Spearmans γ = -0.82; p < 0.05).ConclusionsExamination of the distribution of malaria during 10 years indicated transmission varied among geographic areas and among seasons. Additional studies are needed to examine, in more detail, the association between environmental and meteorological factors and malaria transmission. Furthermore, the role of An. darlingi in malaria transmission in Stann Creek needs further study since, of the three main vectors in Belize, An. darlingi has been found strongly associated with rivers.

Use of Remote Sensing and Geographic Information Systems to Predict Locations of Anopheles darlingi-Positive Breeding Sites Within the Sibun River in Belize, Central America

Abstract Previous studies have identified several anopheline species integral to the transmission of malaria in Belize. The highly efficient vector, Anopheles darlingi Root, is currently considered the most important. The preferred larval habitat of An. darlingi has been described as floating detritus patches, which are commonly associated with overhanging spiny bamboo, Guadua longifolia (E. Fourn.), along river margins. The objectives of this study were to use remote sensing and geographic information system (GIS) tools to 1) define the landscape features (i.e., river curvature, land cover, and house locations) associated with An. darlingi-positive breeding habitats and 2) determine the association between cleared land cover and the growth of spiny bamboo. A systematic survey was conducted in which all detritus patches of at least 1 m2 were sampled, mapped using GPS, and characterized by cause of habitat lodging. Bamboo stretches growing along the river margins also were mapped. Spatial analyses of satellite imagery found no associations between river characteristics or land cover with positive An. darlingi habitats. In addition, there was no significant difference in cleared versus forested land cover in relation to the presence or absence of bamboo. Results indicate that the average distance from homes to negative habitats was significantly greater than from positive detritus mats. Based on the land cover and river characteristics used, our results do not support the use of remote sensing as a predictive tool to locate specific areas within rivers positive for An. darlingi habitats.

The relationship between mosquito abundance and rice field density in the Republic of Korea

BackgroundJapanese encephalitis virus (JEV), the causative agent of Japanese encephalitis (JE), is endemic to the Republic of Korea (ROK) where unvaccinated United States (U.S.) military Service members, civilians and family members are stationed. The primary vector of the JEV in the ROK is Culex tritaeniorhynchus. The ecological relationship between Culex spp. and rice fields has been studied extensively; rice fields have been shown to increase the prevalence of Cx. tritaeniorhynchus. This research was conducted to determine if the quantification of rice field land cover surrounding U.S. military installations in the ROK should be used as a parameter in a larger risk model that predicts the abundance of Cx. tritaeniorhynchus populations.Mosquito data from the U.S. Forces Korea (USFK) mosquito surveillance program were used in this project. The average number of female Cx. tritaeniorhynchus collected per trap night for the months of August and September, 2002-2008, was calculated. Rice fields were manually digitized inside 1.5 km buffer zones surrounding U.S. military installations on high-resolution satellite images, and the proportion of rice fields was calculated for each buffer zone.ResultsMosquito data collected from seventeen sample sites were analyzed for an association with the proportion of rice field land cover. Results demonstrated that the linear relationship between the proportion of rice fields and mosquito abundance was statistically significant (R2 = 0.62, r = .79, F = 22.72, p < 0.001).ConclusionsThe analysis presented shows a statistically significant linear relationship between the two parameters, proportion of rice field land cover and log10 of the average number of Cx. tritaeniorhynchus collected per trap night. The findings confirm that agricultural land cover should be included in future studies to develop JE risk prediction models for non-indigenous personnel living at military installations in the ROK.

Identifying the effective concentration for spatial repellency of the dengue vector Aedes aegypti

BackgroundCurrent efforts are underway to quantify the chemical concentration in a treated air space that elicits a spatial repellent (deterrent) response in a vector population. Such information will facilitate identifying the optimum active ingredient (AI) dosage and intervention coverage important for the development of spatial repellent tools – one of several novel strategies being evaluated for vector-borne disease control. This study reports initial findings from air sampling experiments conducted under field conditions to describe the relationship between air concentrations of repellent AIs and deterrent behavior in the dengue vector, Aedes aegypti.MethodsAir samples were taken inside and outdoors of experimental huts located in Pu Tuey Village, Kanchanaburi Province, Thailand in conjunction with mosquito behavioral evaluations. A mark-release-recapture study design using interception traps was used to measure deterrency of Ae. aegypti against 0.00625% metofluthrin coils and DDT-treated fabric (2g/m2) within separate experimental trials. Sentinel mosquito cohorts were positioned adjacent to air sampling locations to monitor knock down responses to AI within the treated air space. Air samples were analyzed using two techniques: the U.S. Environmental Protection Agency (USEPA) Compendium Method TO-10A and thermal desorption (TD).ResultsBoth the USEPA TO-10A and TD air sampling methods were able to detect and quantify volatized AIs under field conditions. Air samples indicated concentrations of both repellent chemicals below thresholds required for toxic responses (mortality) in mosquitoes. These concentrations elicited up to a 58% and 70% reduction in Ae. aegypti entry (i.e., deterrency) into treated experimental huts using metofluthrin coils and DDT-treated fabric, respectively. Minimal knock down was observed in sentinel mosquito cohorts positioned adjacent to air sampling locations during both chemical evaluations.ConclusionsThis study is the first to describe two air sampling methodologies that are appropriate for detecting and quantifying repellent chemicals within a treated air space during mosquito behavior evaluations. Results demonstrate that the quantity of AI detected by the mosquito vector, Ae. aegypti, that elicits repellency is far lower than that needed for toxicity. These findings have important implications for evaluation and optimization of new vector control tools that function through mosquito behavior modification as opposed to mortality.

Distribution of Anopheles albimanus, Anopheles vestitipennis, and Anopheles crucians Associated with Land Use in Northern Belize

Abstract Anthropogenic land use changes often alter natural patterns of disease transmission. The goal of this study was to determine whether phosphorus input from sugarcane, Saccharum officinarum L., cultivation in northern Belize could pose a significant environmental impact on malaria transmission by changing vegetation structure and composition of wetlands and associated larval habitats. Our primary focus was on the increased dominance of cattail, Typha domingensis Pers., a favored habitat for Anopheles vestitipennis Dyar & Knab. A land cover classification based on satellite imagery was used to select 20 marshes impacted by agricultural runoff and 20 marshes surrounded by forest (nonimpacted). A 100-m transect was established into each of the 40 marshes. Water, vegetation, and larval sampling were conducted at the 0-, 10-, 25-, 50-, and 100-m locations along the transect. Analyses of larval density data indicated that Anopheles albimanus Wiedemann was negatively correlated with percentage of cover of Typha (R2 = 0.39, P < 0.001) but positively correlated with sparse Eleocharis cellulosa Torr. (rush) cover (R2 = 0.19, P < 0.05) and presence of cyanobacterial mats (CBM) (R2 = 0.33, P < 0.0001). An. vestitipennis was found to be positively correlated with percentage of cover of Typha (R2 = 0.19, P < 0.001). Canonical correspondence analysis identified CBM and light as the variables associated with the presence of An. albimanus larvae, Typha cover with An. vestitipennis larvae, and Eleocharis and absence of light with Anopheles crucians (Wiedemann). A positive correlation also existed between marshes adjacent to agricultural activities and presence of An. vestitipennis (R2 = 0.37, P < 0.05). These results indicate that marshes in proximity to agricultural fields are conducive for Typha growth, thereby providing habitat for the more efficient malaria vector An. vestitipennis.

Swine trichinella infection and geographic information system tools.

Pastured pigs are vulnerable to Trichinella spiralis infection through exposure to wild reservoir hosts. To evaluate the potential impact of the expanding production of pork from pasture-raised pigs, we mapped locations of T. spiralis occurrence and pastured-pig farms in the United States. Twenty-eight farms were located within 50 km of previous infection.

Predicted Geographic Ranges for North American Sylvatic Trichinella Species

Abstract Because of a lack of comprehensive surveys, the geographic distributions of the North American species of encapsulating Trichinella (T. nativa and its variant T6, T. murrelli, and T. spiralis) are poorly characterized in detail. These species are potentially zoonotic; therefore, biogeographic information is critical to monitoring their status and any distribution changes due to climatic and man-made environmental impacts. The maximum entropy (Maxent) program was used to model predicted ranges for these sylvatic Trichinella spp., using a limited number of available location records with confirmed species identifications collected over 55 yr throughout North America. The resulting prediction models were shown to be robust, and the species maps created are presented. The predicted range of T. nativa is primarily north of the 48°–52° latitudes, overlapping the Tundra, sub-Arctic, and Warm Continental eco-regions. Its sympatric genotypic variant, T6, has a predicted range covering primarily the sub-Arctic and mountainous Temperate Steppe eco-regions, the latter extending below 48°N latitude. In the east, the T6 range includes the Warm Continental and the mountainous Hot Continental eco-regions; the T6 range is also predicted to extend to the Sierra Madre Mountains of Mexico. The most probable range of T. murrelli is centered in the Midwest within the Hot Continental and Prairie eco-regions, with an extension southward to the Subtropical and Tropical/Subtropical Steppe and Desert eco-regions. In the west, it exists in a restricted range characterized as mountainous Mediterranean. The most probable distribution of sylvatic T. spiralis is along the humid east North American coast (Hot Continental south to Subtropical), and along the coast of northwest North America (Marine) to Alaska (sub-Arctic and Tundra). Its most southerly range extends into central Mexico (Tropical/Subtropical Desert). The difference in relative freeze resistance between T. nativa/T6 and T. murrelli undoubtedly accounts for much of this geographic separation. However, the factors responsible for the absence of a more southerly distribution of T. nativa are not obvious, given the overlap in host range with T. murrelli. The maximum July temperature appears to have a significant effect on this distribution pattern. The results of the model building highlight subjects for future research on the biotic and abiotic factors important in determining Trichinella spp. distributions and directions for model validation research.