The Companion Animal Parasite Council hosted a meeting to identify quantifiable factors that can influence the prevalence of tick-borne disease agents among dogs in North America. This report summarizes the approach used and the factors identified for further analysis with mathematical models of canine exposure to tick-borne pathogens.
Dogs in the United States (USA) are hosts to a diverse range of ixodid ticks and can become infected with many of the pathogens transmitted by these vectors. Advances in diagnostic test and recording technologies have led to the creation of a monthly dataset containing county-by-county canine test results from across the USA. The Companion Animal Parasite Council (CAPC) has assembled large datasets of such results from commercial laboratories that provide diagnostic tests for canine exposure to
Canine diagnostic test results for exposure to tick-borne pathogens, including
Large datasets have been assembled from reports of diagnostic test results for canine exposure to
The overall objective of this CAPC-sponsored workshop was to identify factors that are likely to influence the seroprevalence of canine exposure to tick-borne disease agents in the USA, specifically focusing on the factors and the pathogens for which sufficient data are available, so that these factors could be evaluated for incorporation in mathematical models designed to monitor and to predict spatial and temporal seroprevalence patterns. These preliminary factors provided statisticians some of the critical information needed to begin their model-building procedures.
Two teams of researchers, from various areas of tick and tick-borne pathogen biology, were assembled and tasked with rational identification of factors thought to be relevant to the canine seroprevalence of pathogens transmitted by prostriate (eight team members) or metastriate (seven team members) ticks (Figure
The working groups for both ixodid subfamilies began by discussing variables categorized as (1) vector, (2) host, (3) abiotic, (4) habitat or (5) social. Both groups independently identified numerous factors. The majority of factors were thought to be associated with canine exposure to pathogens vectored by either ixodid subfamily; however, several factors specifically associated with the different ixodid subfamilies also emerged. Variables were also discussed for which there is little or inconsistent supporting data, but these factors could become useful if the data became available. However, in accordance with the workshop objectives, factors for which sufficient data are currently available were chosen for ranking by consensus of each working group.
The variables independently identified by each panel were categorized into the five groups previously indicated (i.e., vector, host, abiotic, habitat and social). Factors regarding exposure to infectious agents transmitted by prostriate ticks were heavily influenced by the preponderance of research on the phenology of
Vector factors Distribution Abundance % Infected Canine contact Local phenology Tolerance to temperature and humidity Activity Focus on adults as primary vector to dogs Host seeking behavior Host contact Feeding preferences and opportunities Deer population drives tick abundance Small mammal population drives infection prevalence Lack of lizards Diversity/dilution effect Tick encounters Questing behavior versus relative humidity Peridomestic encounters – access to areas Urbanization/Rate of development Infection status (decreased survival versus increased cold tolerance)
Presence and abundance (deer, small mammals, lizards) Dilution effect/host diversity Habitat availability and quality Mast crop as a surrogate for host reproduction/fitness Migratory bird patterns Reproductive capacity and timing of vertebrate host reproduction Population control programs in place locally Abiotic host survival factors Temperature, water availability, substrate/nesting material, snow cover Feeding preferences Herd immunity of reservoir host populations Hunting pressure/success Number of deer killed per county – harvest rates Hunting license versus hunting harvest – how active hunting is for that area Hunting limits due to development
Snow cover – depth, duration Miles of roads – neighborhood roads (non-interstate/parkway/highway), trails Soil type – clay versus sand in Northeastern USA Hydrological features
Maximum temperature, warmest month Annual precipitation
Minimum temperature, coldest month Daily temperature (high, low and average) Relative humidity (average, high, low, duration)
Land cover classification Urbanization in 3 categories – low, medium, high Rate of change Forest cover Land cover classification (categorical), % canopy cover, NDVI, EVI (canopy structure) Crop phenology – maximum greening, minimum greening – when greening is happening Supervised vs unsupervised satellite imagery, derived data not currently off the shelf Forest type, forest fragmentation, forest edge length, forest composition, forest connectivity Forest fragments within X distance of road or urban area, close to population centers Understory- could be modeled but is not measured Detritus layers/leaf litter Targeted for future research but perhaps not currently available dataset Soil maps/soil types World harmonized soil database Classification scheme Proximity to rivers/drainage areas Proximity to coast Rain shadows Rivers and streams Attract hosts Serve as corridors Provide humidity Aspect/slope/topo index – derived from digital elevation models, available from hydro dataset More nymphal deer ticks on north- and east-facing slopes Effective distance – more ticks on uphill side of a payout Ticks associated with east-facing woodland edges that slope down to water Fire Eliminates leaf litter, changes food availability, changes microclimate Depending on timing, burn can increase number of infected ticks, so fewer ticks but higher infection rate Park boundaries – proximity to parks
Human population centers Dog ownership, dog lifestyle Hunting styles that use dogs Breed of dog Dog ownership increase – by region More homes in tick habitat – demographic factors Deer/vehicle collisions – deer crossing signs Acaricide use/quality of care for dogs Average household income Presence of clinics, proximity to clinics, number of vet clinics in an area, size of clinics Cultural – forest foraging (mushroom hunting in Missouri) Internet use Social media Smartphone use Education level Population density Housing type (average lot size, median home price, age of house unit, census tract size) Vector factors Biology Competence (different transmission scenarios) Host preference Persistence and interhost transfer of male ticks Host seeking behavior (hunt, ambush) Population dynamics Distribution (established, intermittent or absent) Relative abundance (species and stages) Seasonality Different stages Stage overlap
Principal host(s) of different tick stages Susceptibility to pathogen Distribution Density-Dynamic Ecologic diversity (dilution effect) Shannon-Weaver Index Tick-permissive, non-reservoir hosts Behavior Host grooming Gregariousness Host species Home Range Migration, dispersal Anthropogenic translocation Hosts permissive for pathogen Persistence in reservoir Prevalence of infection Density Other transmission routes Life cycle/age distribution Immune response Amplification vs. reservoir Domestic Indoor/outdoor Rural/urban Relocation Sylvatic vs. Suburban Opportunistic or natural infection
Humidity Maximum, minimum and average Temperature Maximum, minimum and average Degree-day Soil temperature Photoperiod Seasonal precipitation El Niño effect Snow and other ground cover Catastrophic disturbance Fire Hurricane Wind Altitude
Macrohabitat Vegetation (density, type and fragmentation) Elevation Location of water sources Rainfall Microhabitat Soil type LIDAR data Land use
Land use Indoor versus outdoor dogs Dog use ( Canine husbandry Use of tick preventives Nuisance permits Housekeeping Animal welfare violations Socioeconomics Average household income Human population Large-scale economic factors Recreation Hunting Parks (rural and urban) Pets per household
The geographic distribution of prostriate ticks was focused on the
Defining permanent values of tick abundance levels is problematic, because tick population levels within a given area are temporally and spatially variable and can change rapidly. Tick abundance depends on host abundance and availability, relative humidity, precipitation and temperature, and can reflect conditions from previous years when immature tick stages or prior generations were active.
Activity is indicative of questing behavior, host-seeking behavior, host contact and the feeding preferences of different developmental stages. The presence of ticks in an area is not alone indicative of activity. For example, tick activity will depend on temperature, precipitation, relative humidity and photoperiod.
The deer population is a major driver of abundance for certain ticks, such as
Rodents are an important component of the ecologies of several tick species and some tick-borne infectious agents. Immature stages of several tick species acquire blood meals from small vertebrate hosts. Several tick-borne infectious agents, such as
Small vertebrates such as lizards, which are permissive hosts for immature tick stages but are not definitively documented reservoirs of the pathogens under consideration, could dampen transmission of disease agents that are adapted to rodent reservoirs. Conversely, removal of lizards reportedly reduced nymphal tick numbers from an environment but did not affect the percentage of
Migratory birds can introduce some tick species to new areas [
Different tick species and their natural hosts can be adapted to various environments that are influenced by abiotic factors such as precipitation, temperature, relative humidity and soil composition.
Factors that influence the life cycles of ticks and their vertebrate hosts include vegetation, urbanization, land use in non-urban settings and detritus layers.
Human behavior and population characteristics influence the exposure of dogs to ticks. These include access to preventive care, recreation, socioeconomic status, income, pathogen reservoir control, vector-amplification host control and news media coverage.
A number of variables were discussed for which comprehensive, nationwide data did not seem currently available. These variables included vector infection rates, detailed reservoir infection rates, vector abundances, vector efficiency indices, vector survival, vectorial capacities, temperature-dependent development rates of vectors (natural temperature regimes), total number of dogs (by county or zip code) and tick control product sales in each geographic region. Local data may be available for some of these variables in certain areas, but national datasets were not available at the time of this meeting.
Each expert panel was asked to prioritize 10 factors most expected to drive a reliable mathematical predictive model. These lists, summarized in Tables
aSimilar variables also ranked by the metastriate-borne pathogen panel.
aVariables also ranked by the prostriate-borne pathogen panel.
bVariables shared among all ixodid ticks considered for this report.1. Forest cover/NDVI or EVIa
2. Relative humidity 3. Annual precipitation (including snow cover)a
4. Human population densitya
5. Deer/vehicle collisionsa
6. Topography/altitude/aspect 6. Temperature – max warmest, min coldesta
7. Proximity of forest to impervious surfaces or roads/built environment 8. Human case distribution 8. Distribution/abundance of 9. Household incomea
10. Forest fragmentation indexa
Majority of the metastriata: 1. Vector distribution (established, intermittent or absent)a
2. Maximum, minimum and average temperatureb
3. Amount of precipitationa
4. LiDAR (up to 6 layers) 5. GAP/categorical analysis of vegetationa
6. Reservoir host densitiesa
7. Human population (census)a,b
8. Median household incomea,b
9. Fragmentation of vegetationb
10. Degree-days 11. Seasonal precipitation (snow cover)a
1. Median household income a,b
2. Registered dog breeders (kennels, puppy mills, 3. Human population (census)a,b
4. Tick preventive sales 5. Animal welfare violations 6. Latitude
The prevalence data at the foundation of this predictive model is largely based on serodiagnostic tests. Although seropositivity is reflective of past exposure, it does not demonstrate recent or active infections. Repeatedly seropositive samples from the same dogs at different times are also to be occasionally expected, because some dogs may have tested seropositive in previous tests and because some tests are conducted to monitor host responses to treatment. Travel histories and certainties of the individual test results are currently unavailable for the dogs reported in this dataset.
An analogous project for mathematical modeling of the prevalence of canine heartworm was simultaneously undertaken by CAPC [
Attempts to fit the seroprevalence of
This meeting brought together a range of junior and senior scientists engaged in various aspects of research in the biology of ticks and tick-borne infections. The specific objectives were to identify and to prioritize quantifiable factors expected to contribute to canine exposure to organisms transmitted by the two major subfamilies of ixodid ticks. The two panels ranked 12 and 17 factors associated with prostriate and metastriate ixodid ticks, respectively. Eight of these factors were independently prioritized by both panels; four of 12 factors were unique to prostriate-vectored agents, two of 11 factors were unique to metastriate-vectored agents transmitted by ticks other than
The authors have no competing interests relative to the work presented in this report.
SEL, DDB, CL, CC, RL and RWS conceived of and organized the meeting that generated the information provided in this report. BLB, DDB, CC, MRC, SAE, DF, JEF, HG, GJH, RRL, SEL, CL, RL, TM, GRN, WLN, JS, RWS, AV-S and DW participated in the meeting and contributed to the identification of candidate factors. RWS tabulated the candidate factors from the meeting minutes, and SEL, DDB and RWS generated the initial draft of the manuscript. RWS was responsible for distribution of the manuscript to the co-authors, for revision in response to comments, and for formatting the final manuscript version for submission. All authors read and approved the final version of the manuscript.
This meeting was supported by the Companion Animal Parasite Council (CAPC), and we are grateful to Sonya Hennessy for assistance in organizing and hosting this meeting. The CAPC is in turn grateful to its sponsors that provide data for Parasite Prevalence Maps: the IDEXX, Antech, Banfield and Abaxis corporations. We are also grateful to the veterinarians across the USA who test their patients for exposure to vector-borne pathogens, especially those who report test results that can eventually be included as data in the CAPC Parasite Prevalence Maps. Robert Lund acknowledges support from the CAPC and from the National Science Foundation Grant DMS-1407480. The opinions and assertions contained herein are those of the authors and are not to be construed as official or reflecting the views of the Department of the Army or the Department of Defense.