Quantitative factors proposed to influence the prevalence of canine tick-borne disease agents in the United States
- Roger W Stich1Email author,
- Byron L Blagburn2,
- Dwight D Bowman3,
- Christopher Carpenter4,
- M Roberto Cortinas5,
- Sidney A Ewing6,
- Desmond Foley7,
- Janet E Foley8,
- Holly Gaff9,
- Graham J Hickling10,
- R Ryan Lash11,
- Susan E Little6,
- Catherine Lund12,
- Robert Lund13,
- Thomas N Mather14,
- Glen R Needham15,
- William L Nicholson16,
- Julia Sharp13,
- Andrea Varela-Stokes17 and
- Dongmei Wang13
© Stich et al.; licensee BioMed Central Ltd. 2014
Received: 19 August 2014
Accepted: 30 August 2014
Published: 4 September 2014
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.
KeywordsAnaplasma Ehrlichia Borrelia burgdorferi Tick-borne infections Prevalence map factors Ticks Ixodidae Prostriata Metastriata
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 Borrelia burgdorferi, Ehrlichia spp. and Anaplasma spp. . These monthly, county-level CAPC prevalence maps generated interest in the utility of the datasets for assessing seroprevalence norms, forecasting future seroprevalence rates and for identifying trends in canine exposure to this array of tick-borne disease agents. A group of vector ecologists, parasitologists, other biologists and statistical modelers met in Atlanta, GA (June 9–10, 2012) to identify factors that could enhance the accuracy of these predictive models. This report narrates the results of the meeting.
Canine diagnostic test results for exposure to tick-borne pathogens, including B. burgdorferi, Ehrlichia spp. and Anaplasma spp., are of significant interest, not only because canine health is important to pet owners and veterinarians, but also because of the public health importance of many of these infectious disease agents. These tick-borne pathogens are transmitted by two phylogenetically distinct groups of ixodid ticks. Members of the ixodid subfamily Prostriata (Ixodes spp.) transmit agents of granulocytic anaplasmosis (Anaplasma phagocytophilum) and Lyme borreliosis (B. burgdoferi) and are likely to include vectors of a more recently described Ehrlichia muris-like agent in the USA. Members of the subfamily Metastriata (e.g., the genera Amblyomma, Dermacentor and Rhipicephalus) transmit agents of canine and human ehrlichiosis (e.g., E. canis, E. chaffeensis and E. ewingii), canine anaplasmosis (A. platys) and spotted-fever group rickettsiosis (i.e., Rickettsia rickettsii, R. conorii and related Rickettsia spp.).
Large datasets have been assembled from reports of diagnostic test results for canine exposure to B. burgdorferi, Anaplasma spp. and Ehrlichia spp. in the USA. For example, from reports submitted nationwide from 2010–2012, 509,195 (7.2%) of 6,996,197 canine samples were seropositive for B. burgdorferi, 270,168 (4.4%) of 6,192,268 samples were seropositive for Anaplasma, and 111,673 (1.1%) of 6,994,683 samples were seropositive for Ehrlichia. A previous national survey, spanning 2001–2007, reported results from 982,336 diagnostic tests for canine exposure to B. burgdorferi and Ehrlichia spp., and 479,640 tests for canine antibodies to Anaplasma spp., with 5.1%, 0.6% and 4.7% of these samples testing seropositive for B. burgdorferi, Ehrlichia and Anaplasma, respectively . Interestingly, when the canine seroprevalence of B. burgdorferi in the 2001–2007 study was compared to the subsequent prevalence of human Lyme disease, the most commonly reported human vector-borne illness in the USA, canine seroprevalence of B. burgdorferi ≥5.1% was predictive of emergent human Lyme disease in low-incidence counties; a low canine seroprevalence (≤1.0%) was associated with minimal risk for emergent human Lyme disease . A subsequent report, however, underscored the importance of other variables, such as the distribution of competent vector species, for accurate interpretation of these canine diagnostic test data .
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.
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.
Factors initially considered as potential contributors to canine prevalence of disease agents transmitted by Ixodes scapularis and I. pacificus
Tolerance to temperature and humidity
Focus on adults as primary vector to dogs
Host seeking behavior
Feeding preferences and opportunities
Deer population drives tick abundance
Small mammal population drives infection prevalence
Lack of lizards
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
Herd immunity of reservoir host populations
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
Maximum temperature, warmest month
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
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
Proximity to rivers/drainage areas
Proximity to coast
Rivers and streams
Serve as corridors
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
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)
Housing type (average lot size, median home price, age of house unit, census tract size)
Factors discussed as potential contributors to seroprevalence of metastriate tick-borne pathogens among dogs in the USA
Competence (different transmission scenarios)
Persistence and interhost transfer of male ticks
Host seeking behavior (hunt, ambush)
Distribution (established, intermittent or absent)
Relative abundance (species and stages)
Principal host(s) of different tick stages
Susceptibility to pathogen
Ecologic diversity (dilution effect)
Tick-permissive, non-reservoir hosts
Hosts permissive for pathogen
Persistence in reservoir
Prevalence of infection
Other transmission routes
Life cycle/age distribution
Amplification vs. reservoir
Sylvatic vs. Suburban
Opportunistic or natural infection
Maximum, minimum and average
Maximum, minimum and average
El Niño effect
Snow and other ground cover
Vegetation (density, type and fragmentation)
Location of water sources
Indoor versus outdoor dogs
Dog use (e.g., hunting)
Use of tick preventives
Animal welfare violations
Average household income
Large-scale economic factors
Parks (rural and urban)
Pets per household
The geographic distribution of prostriate ticks was focused on the Ixodes spp. thought to most commonly feed on dogs (and people) in the USA: I. scapularis and I. pacificus. Metastriate ticks considered as pathogen vectors (e.g., of Ehrlichia spp. and A. platys) included, in alphabetical order, A. americanum, A. maculatum, D. andersoni, D. variabilis and R. sanguineus. The general distributions of these ticks are relatively well documented in the literature and via voucher specimens in the USA. However, the spatial resolutions of these data vary in different regions, and defining the minimum useful scale can be complicated by discontinuous geographic distributions of tick populations in a given area.
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 I. scapularis, I. pacificus and A. americanum. Deer are also a reservoir of E. chaffeensis and could be involved in the maintenance of E. ewingii.
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 B. burgdorferi, A. phagocytophilum and R. rickettsii are adapted to rodent reservoir hosts.
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 B. burgdorferi-positive ticks, suggesting that increased numbers of lizard hosts might actually increase the risk of pathogen transmission by serving to increase the overall number of ticks in a given area .
Migratory bird patterns
Migratory birds can introduce some tick species to new areas . However, ticks that feed on dogs and that are dispersed by birds in the USA may be incapable of maintaining an active population cycle in the absence of larger vertebrate hosts (e.g., white-tailed deer).
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.
Ranked factors identified for canine seroprevalence models of infections transmitted by Ixodes spp. in the USA
Forest cover/NDVI or EVIa
Annual precipitation (including snow cover)a
Human population densitya
Temperature – max warmest, min coldesta
Proximity of forest to impervious surfaces or roads/built environment
Human case distribution
Distribution/abundance of I. scapularis and I. pacificusa
Forest fragmentation indexa
Ranked factors for preliminary models of metastriate tick-borne pathogen prevalence among dogs in the USA
Majority of the metastriata:
Vector distribution (established, intermittent or absent)a
Maximum, minimum and average temperatureb
Amount of precipitationa
LiDAR (up to 6 layers)
GAP/categorical analysis of vegetationa
Reservoir host densitiesa
Human population (census)a,b
Median household incomea,b
Fragmentation of vegetationb
Seasonal precipitation (snow cover)a
Median household income a,b
Registered dog breeders (kennels, puppy mills, etc.)
Human population (census)a,b
Tick preventive sales
Animal welfare violations
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 [8, 9], and each prioritized factor identified by the expert panel had significant predictive power with ≥95% confidence. Overall, the model explained 60%-70% of variability in the CAPC county-by-county dataset from 2011–2013. Similarly, preliminary analysis of canine seroprevalence of Anaplasma spp. indicated that temperature, precipitation, relative humidity, population density, median household income, forestation coverage, elevation and deer/vehicle strike rates were significant with ≥95% confidence, and that the total proportion of variability explained in the 2011–2013 data is around 60-70% . Thus, the prevalence of heartworm and seroprevelance of Anaplasma among dogs appear amenable to quantification that could facilitate monitoring for outbreaks, remediation of vector abundance or for forecasting future seroprevalence levels.
Attempts to fit the seroprevalence of B. burgdorferi and of Ehrlichia spp. among dogs are also underway, with mixed results. The spatial seroprevalence of B. burgdorferi among dogs has been similar to and appears to be as quantifiable as that of Anaplasma spp. Conversely, the canine seroprevalence of Ehrlichia spp. appears to be highly variable, with some neighboring areas reporting antipodal seroprevalence rates that could be reflective of vector ecology or social factors. Future work will address these issues.
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 R. sanguineus, and four of six factors were unique to agents vectored by R. sanguineus. The next phase of this project will move from rational identification of perceived factors to statistical assessment of factors for predictive power. Forecasting issues will also be explored.
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.
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