Reported County-Level Distribution of Lyme Disease Spirochetes, Borrelia burgdorferi sensu stricto and Borrelia mayonii (Spirochaetales: Spirochaetaceae), in Host-Seeking Ixodes scapularis and Ixodes pacificus Ticks (Acari: Ixodidae) in the Contiguous United States.

Lyme disease is the most common vector-borne disease in the United States. While Lyme disease vectors are widespread, high incidence states are concentrated in the Northeast, North Central and Mid-Atlantic regions. Mapping the distribution of Lyme disease spirochetes in ticks may aid in providing data-driven explanations of epidemiological trends and recommendations for targeting prevention strategies to communities at risk. We compiled data from the literature, publicly available tickborne pathogen surveillance databases, and internal CDC pathogen testing databases to map the county-level distribution of Lyme disease spirochetes reported in host-seeking Ixodes pacificus and Ixodes scapularis across the contiguous United States. We report B. burgdorferi s.s.-infected I. scapularis from 384 counties spanning 26 eastern states located primarily in the North Central, Northeastern, and Mid-Atlantic regions, and in I. pacificus from 20 counties spanning 2 western states, with most records reported from northern and north-coastal California. Borrelia mayonii was reported in I. scapularis in 10 counties in Minnesota and Wisconsin in the North Central United States, where records of B. burgdorferi s.s. were also reported. In comparison to a broad distribution of vector ticks, the resulting map shows a more limited distribution of Lyme disease spirochetes.

Benefits and Drawbacks of Citizen Science to Complement Traditional Data Gathering Approaches for Medically Important Hard Ticks (Acari: Ixodidae) in the United States.

Tick-borne diseases are increasing in North America. Knowledge of which tick species and associated human pathogens are present locally can inform the public and medical community about the acarological risk for tick bites and tick-borne infections. Citizen science (also called community-based monitoring, volunteer monitoring, or participatory science) is emerging as a potential approach to complement traditional tick record data gathering where all aspects of the work is done by researchers or public health professionals. One key question is how citizen science can best be used to generate high-quality data to fill knowledge gaps that are difficult to address using traditional data gathering approaches. Citizen science is particularly useful to generate information on human-tick encounters and may also contribute to geographical tick records to help define species distributions across large areas. Previous citizen science projects have utilized three distinct tick record data gathering methods including submission of: 1) physical tick specimens for identification by professional entomologists, 2) digital images of ticks for identification by professional entomologists, and 3) data where the tick species and life stage were identified by the citizen scientist. We explore the benefits and drawbacks of citizen science, relative to the traditional scientific approach, to generate data on tick records, with special emphasis on data quality for species identification and tick encounter locations. We recognize the value of citizen science to tick research but caution that the generated information must be interpreted cautiously with data quality limitations firmly in mind to avoid misleading conclusions.

Tick and Tickborne Pathogen Surveillance as a Public Health Tool in the United States.

In recent decades, tickborne disease (TBD) cases and established populations of medically important ticks have been reported over expanding geographic areas, and an increasing number of tickborne bacteria, viruses, and protozoans have been recognized as human pathogens, collectively contributing to an increasing burden of TBDs in the United States. The prevention and diagnosis of TBDs depend greatly on an accurate understanding by the public and healthcare providers of when and where persons are at risk for exposure to human-biting ticks and to the pathogens these ticks transmit. However, national maps showing the distributions of medically important ticks and the presence or prevalence of tickborne pathogens are often incomplete, outdated, or lacking entirely. Similar deficiencies exist regarding geographic variability in host-seeking tick abundance. Efforts to accurately depict acarological risk are hampered by lack of systematic and routine surveillance for medically important ticks and their associated human pathogens. In this review, we: 1) outline the public health importance of tick surveillance; 2) identify gaps in knowledge regarding the distributions and abundance of medically important ticks in the United States and the presence and prevalence of their associated pathogens; 3) describe key objectives for tick surveillance and review methods appropriate for addressing those goals; and 4) assess current capacity and barriers to implementation and sustainability of tick surveillance programs.

Preliminary Evaluation of Human Personal Protective Measures Against the Nymphal Stage of the Asian Longhorned Tick (Acari: Ixodidae).

The invasive, human-biting Asian longhorned tick, Haemaphysalis longicornis Neumann, is establishing in the United States. This tick is a threat to public health in its native range in Asia, serving as a vector of severe fever with thrombocytopenia syndrome virus and Rickettsia japonica, the agent of Japanese spotted fever. However, there is a lack of published information specifically for H. longicornis concerning the efficacy of generally recommended personal tick bite prevention measures. We, therefore, evaluated permethrin-treated clothing and formulated human skin repellent products, representing the six repellent active ingredients generally recommended for tick bite prevention by the Centers for Disease Control and Prevention (CDC), against H. longicornis nymphs from a colony established with adult ticks collected in New York state. Reluctance of H. longicornis nymphs to stay in contact with nontreated human skin precluded the use of a human skin bioassay to optimally evaluate repellency. In a Petri dish choice bioassay, all tested product formulations were highly effective with estimated repellencies ranging from 93 to 97%. In addition, we observed strong contact irritancy of a summer-weight permethrin-treated garment against H. longicornis nymphs, with 96% of introduced ticks dislodging from the vertically oriented textile within 3 min. These preliminary studies indicate that personal tick bite prevention measures currently recommended by the CDC are effective against the invasive H. longicornis. However, additional studies are needed to explore the efficacy of the evaluated products against different life stages of H. longicornis, as well as ticks collected in the field rather than reared in the laboratory.

An Evaluation of the Flea Index as a Predictor of Plague Epizootics in the West Nile Region of Uganda.

Plague is a low incidence flea-borne zoonosis that is often fatal if treatment is delayed or inadequate. Outbreaks occur sporadically and human cases are often preceded by epizootics among rodents. Early recognition of epizootics coupled with appropriate prevention measures should reduce plague morbidity and mortality. For nearly a century, the flea index (a measure of fleas per host) has been used as a measure of risk for epizootic spread and human plague case occurrence, yet the practicality and effectiveness of its use in surveillance programs has not been evaluated rigorously. We sought to determine whether long-term monitoring of the Xenopsylla flea index on hut-dwelling rats in sentinel villages in the plague-endemic West Nile region of Uganda accurately predicted plague occurrence in the surrounding parish. Based on observations spanning ~6 yr, we showed that on average, the Xenopsylla flea index increased prior to the start of the annual plague season and tended to be higher in years when plague activity was reported in humans or rodents compared with years when it was not. However, this labor-intensive effort had limited spatial coverage and was a poor predictor of plague activity within sentinel parishes.

Reported County-Level Distribution of the American Dog Tick (Acari: Ixodidae) in the Contiguous United States.

In the United States, tick-borne diseases are increasing in incidence and cases are reported over an expanding geographical area. Avoiding tick bites is a key strategy in tick-borne disease prevention, and this requires current and accurate information on where humans are at risk for exposure to ticks. Based on a review of published literature and records in the U.S. National Tick Collection and National Ecological Observatory Network databases, we compiled an updated county-level map showing the reported distribution of the American dog tick, Dermacentor variabilis (Say). We show that this vector of the bacterial agents causing Rocky Mountain spotted fever and tularemia is widely distributed, with records derived from 45 states across the contiguous United States. However, within these states, county-level records of established tick populations are limited. Relative to the range of suitable habitat for this tick, our data imply that D. variabilis is currently underreported in the peer-reviewed literature, highlighting a need for improved surveillance and documentation of existing tick records.

Experimental Demonstration of Reservoir Competence of the White-Footed Mouse, Peromyscus leucopus (Rodentia: Cricetidae), for the Lyme Disease Spirochete, Borrelia mayonii (Spirochaetales: Spirochaetaceae).

The white-footed mouse, Peromyscus leucopus (Rafinesque), is a reservoir for the Lyme disease spirochete Borrelia burgdorferi sensu stricto in the eastern half of the United States, where the blacklegged tick, Ixodes scapularis Say (Acari: Ixodidae), is the primary vector. In the Midwest, an additional Lyme disease spirochete, Borrelia mayonii, was recorded from naturally infected I. scapularis and P. leucopus. However, an experimental demonstration of reservoir competence was lacking for a natural tick host. We therefore experimentally infected P. leucopus with B. mayonii via I. scapularis nymphal bites and then fed uninfected larvae on the mice to demonstrate spirochete acquisition and passage to resulting nymphs. Of 23 mice fed on by B. mayonii-infected nymphs, 21 (91%) developed active infections. The infection prevalence for nymphs fed as larvae on these infected mice 4 wk post-infection ranged from 56 to 98%, and the overall infection prevalence for 842 nymphs across all 21 P. leucopus was 75% (95% confidence interval, 72-77%). To assess duration of infectivity, 10 of the P. leucopus were reinfested with uninfected larval ticks 12 wk after the mice were infected. The overall infection prevalence for 480 nymphs across all 10 P. leucopus at the 12-wk time point was 26% (95% confidence interval, 23-31%), when compared with 76% (95% confidence interval, 71-79%) for 474 nymphs from the same subset of 10 mice at the 4-wk time point. We conclude that P. leucopus is susceptible to infection with B. mayonii via bite by I. scapularis nymphs and an efficient reservoir for this Lyme disease spirochete.

Modeling Climate Suitability of the Western Blacklegged Tick in California.

Ixodes pacificus Cooley & Kohls (Acari: Ixodidae), the primary vector of Lyme disease spirochetes to humans in the far-western United States, is broadly distributed across Pacific Coast states, but its distribution is not uniform within this large, ecologically diverse region. To identify areas of suitable habitat, we assembled records of locations throughout California where two or more I. pacificus were collected from vegetation from 1980 to 2014. We then employed ensemble species distribution modeling to identify suitable climatic conditions for the tick and restricted the results to land cover classes where these ticks are typically encountered (i.e., forest, grass, scrub-shrub, riparian). Cold-season temperature and rainfall are particularly important abiotic drivers of suitability, explaining between 50 and 99% of the spatial variability across California among models. The likelihood of an area being classified as suitable increases steadily with increasing temperatures >0°C during the coldest quarter of the year, and further increases when precipitation amounts range from 400 to 800 mm during the coldest quarter, indicating that areas in California with relatively warm and wet winters typically are most suitable for I. pacificus. Other consistent predictors of suitability include increasing autumn humidity, temperatures in the warmest month between 23 and 33°C, and low-temperature variability throughout the year. The resultant climatic suitability maps indicate that coastal California, especially the northern coast, and the western Sierra Nevada foothills have the highest probability of I. pacificus presence.

Prevalence and Geographic Distribution of Borrelia miyamotoi in Host-Seeking Ixodes pacificus (Acari: Ixodidae) Nymphs in Mendocino County, California.

Borrelia miyamotoi is an increasingly recognized human pathogen transmitted by Ixodes ticks in the Northern Hemisphere. In North America, infection prevalences of B. miyamotoi are characteristically low (<10%) in Ixodes scapularis (Say; Acari: Ixodidae) and Ixodes pacificus (Cooley & Kohls; Acari: Ixodidae), both of which readily bite humans. We tested 3,255 host-seeking I. pacificus nymphs collected in 2004 from 79 sites throughout Mendocino County in north-coastal California for presence of B. miyamotoi. The collection sites represented a variety of forest types ranging from hot, dry oak woodlands in the southeast, to coastal redwoods in the west, and Ponderosa pine and Douglas fir-dominated areas in the northern part of the county. We found that B. miyamotoi was geographically widespread, but infected I. pacificus nymphs infrequently (cumulative prevalence of 1.4%). Infection prevalence was not significantly associated with geographic region or woodland type, and neither density of host-seeking nymphs, nor infection with Borrelia burgdorferi sensu stricto was associated with B. miyamotoi infection status in individual ticks. Because B. burgdorferi prevalence at the same sites was previously associated with woodland type and nymphal density, our results suggest that despite sharing a common vector, the primary modes of enzootic maintenance for the two pathogens are likely different.

The Role of Early-Phase Transmission in the Spread of Yersinia pestis.

Early-phase transmission (EPT) of Yersinia pestis by unblocked fleas is a well-documented, replicable phenomenon with poorly defined mechanisms. We review evidence demonstrating EPT and current knowledge on its biological and biomechanical processes. We discuss the importance of EPT in the epizootic spread of Y. pestis and its role in the maintenance of plague bacteria in nature. We further address the role of EPT in the epidemiology of plague.

Changing socioeconomic indicators of human plague, New Mexico, USA.

Socioeconomic indicators associated with temporal changes in the distribution of human plague cases in New Mexico were investigated for 1976-2007. In the 1980s, cases were more likely in census block groups with poor housing conditions, but by the 2000s, cases were associated with affluent areas concentrated in the Santa Fe-Albuquerque region.

Climatic predictors of the intra- and inter-annual distributions of plague cases in New Mexico based on 29 years of animal-based surveillance data.

Within the United States, the majority of human plague cases are reported from New Mexico. We describe climatic factors involved in intra- and inter-annual plague dynamics using animal-based surveillance data from that state. Unlike the clear seasonal pattern observed at lower elevations, cases occur randomly throughout the year at higher elevations. Increasing elevation corresponded with delayed mean time in case presentation. Using local meteorological data (previous year mean annual precipitation, total degrees over 27 degrees C 3 years before and maximum winter temperatures 4 years before) we built a time-series model predicting annual case load that explained 75% of the variance in pet cases between years. Moreover, we found a significant correlation with observed annual human cases and predicted pet cases. Because covariates were time-lagged by at least 1 year, intensity of case loads can be predicted in advance of a plague season. Understanding associations between environmental and meteorological factors can be useful for anticipating future disease trends.

Residence-linked human plague in New Mexico: a habitat-suitability model.

Yersinia pestis, the causative agent of plague, has been detected in fleas and mammals throughout the western United States. This highly virulent infection is rare in humans, surveillance of the disease is expensive, and it often was assumed that risk of exposure to Y. pestis is high in most of the western United States. For these reasons, some local health departments in these plague-affected regions have hesitated to undertake surveillance and other prevention activities. To aid in targeting limited public health resources, we created a fine-resolution human plague risk map for New Mexico, the state reporting more than half the human cases in the United States. Our GIS-based model included three landscape features-a nonlinear relationship with elevation, distance to water, and distance to the ecotone between Rocky Mountain/Great Basin open and closed coniferous woodlands-and yielded an overall accuracy of approximately 80%. The model classified 17.25% of the state as posing significant risk of exposure to humans on privately or tribally owned land, which suggests that resource requirements for regular surveillance and control of plague could be effectively focused on < 20% of the state.