|Year : 2021 | Volume
| Issue : 4 | Page : 352-358
Active surveillance of ticks in peri-domestic areas of Indiana, Midwest United States
Oghenekaro Omodior1, Sina Kianersi2
1 Department of Health and Wellness Design, Indiana University School of Public Health, Bloomington, Indiana, USA
2 Department of Epidemiology and Biostatistics, School of Public Health, Indiana University, Bloomington, Indiana, USA
|Date of Submission||18-Jul-2020|
|Date of Acceptance||15-Apr-2021|
|Date of Web Publication||25-Mar-2022|
Department of Health and Wellness Design, Indiana University School of Public Health, Bloomington Indiana. 47405
Source of Support: None, Conflict of Interest: None
Background & objectives: The incidence of Borreliosis, Anaplasmosis, Babesiosis and other tick-borne diseases acquired from private residential/peri-domestic areas has increased over the decades. However, tick activity and proportion of private residential properties with established tick populations remain unknown. The purpose of the current study was to determine the predictors of tick activity in peri-domestic areas.
Methods: In a cross-sectional study design, we used snowball-sampling with cold-calling techniques to collect free-living ticks, sociodemographic, and microclimatic data from June to November 2018 from a total of 96 private residential areas in south-central Indiana, USA.
Results: Thirty-eight percent of peri-domestic areas sampled had tick activity, and of these, 50% had established tick populations. Nymphal ticks were the most abundant life stage. Self-reported TBD diagnosis was 16%. Amblyomma americanum [Linnaeus (lone star tick)] was the most abundant tick species collected. Other tick species identified include: Ixodes scapularis [Say (black-legged/deer tick)] and Dermacentor variabilis [Say (American dog tick)]. Increasing temperature was positively associated with tick activity, while elevation was negatively associated with tick abundance.
Interpretation & conclusion: Our study results reveal that the proportion of peri-domestic areas in Indiana with established tick populations is high. Amblyomma americanum tick is the most predominant tick species in peri-domestic areas of south-central Indiana. Active surveillance of ticks in peri-domestic areas is necessary for informing decisions by households and communities about where to target tick exposure and tick-borne disease prevention efforts.
Keywords: Tick-borne diseases; peri-domestic areas; Indiana, Midwest United States; Amblyomma americanum; Dermacentor variabilis; Ixodes scapularis
|How to cite this article:|
Omodior O, Kianersi S. Active surveillance of ticks in peri-domestic areas of Indiana, Midwest United States. J Vector Borne Dis 2021;58:352-8
|How to cite this URL:|
Omodior O, Kianersi S. Active surveillance of ticks in peri-domestic areas of Indiana, Midwest United States. J Vector Borne Dis [serial online] 2021 [cited 2022 May 21];58:352-8. Available from: https://www.jvbd.org/text.asp?2021/58/4/352/316271
| Introduction|| |
In less than two decades, the incidence of Anaplasmosis, Borreliosis, Ehrlichiosis Rocky Mountain Spotted Fever and other tick-borne diseases (TBD) in the United States has more than doubled, from 22,527 in 2004 to 47,743 in 2018. This despite the evidence that TBD incidence is highly under-reported nationwide. Active surveillance of ticks using drag sampling and tick baiting provides the most sensitive measure of human risk of tick exposure. This is because exposure to potentially infected ticks is the single most important risk factor for TBD incidence, and a determination of whether tick populations are established at a location is an important indicator of tick exposure risk assessment,. Although multiple studies have demonstrated increased tick activity and TBD infection from peri-domestic areas (i.e., the yard on private residential property) across the United States, the proportion of peri-domestic areas with established tick populations is also unknown,,,,. Although outdoor insecticide application, and creating a tick-safe zone through a combination of landscaping practices are strategies recommended for preventing ticks in the peri-domestic area, their extent of adoption in Indiana is unknown. Currently, active surveillance of ticks in Indiana takes place only in public access lands, while excluding peri-domestic areas. Furthermore, fewer studies have tested the association between residential scale microclimatic factors (i.e., temperature, relative humidity, etc.) and tick activity,,.
In this study, we present the results of the first year of a multiyear active surveillance of ticks and TBD diagnosis in peri-domestic areas of Indiana. Proportion of peri-domestic areas with tick activity and established tick populations, peri-domestic TBD diagnosis, together with the significant microclimatic predictors of tick activity (presence/density) are presented. The current results provide further justification for active surveillance, while shedding some light on the changing risk of tick exposure and TBD in peri-domestic areas. Future project goals include combining these results with data on tick infection prevalence and tick microbiome diversity to estimate TBD risk, and as an early warning system for monitoring the emergence of ticks and novel tick-borne microbes in new locations. Long term, this project is expected to provide a reliable risk map for Indiana and the Midwestern United States, with an estimated population of 70 million people. Such a map can be used as a guide for spatial prioritization of prevention efforts.
| Material & Methods|| |
Data collection occurred from June to November 2018. Ninety-six peri-domestic areas spread across 7 counties in south-central Indiana were sampled [Figure 1]. The counties were selected as part of the first phase of a multi-year tick surveillance project. First group of homeowners were recruited using flyers distributed across various public places. Subsequently, these participants assisted in recruiting other homeowners using a process of snowball-sampling with cold-calling, as long as they met inclusion criteria. All homeowners first completed a brief email or telephone survey to assess if they met inclusion criteria. Peri-domestic areas were included in sampling if they shared some of the following landscape features: 1) adult homeowner/occupier must have lived at the residential property for at least 6 months, 2) peri-domestic area had the presence of leaf litter, wooded or grassy area with vegetative shrubs, understory or canopy trees, 3) residential property was within 30 m of woodland, 4) owner/occupier reports previously observing known tick vertebrate hosts (e.g. deer, grey squirrel, rabbit, groundhog, opossum), and 5) property has not been known to have been treated with acaricide. At each private residential property, we collected sociodemographic data from the adult homeowner, and obtained tick samples and microclimatic data from the corresponding peri-domestic area. In addition to other sociodemographic data, we combined the responses to the following two questions to capture self-reported peri-domestic TBD diagnosis; 1) “Have you ever been diagnosed with a tick-borne disease (e.g., Lyme, Rocky Mountain Spotted Fever, Ehrlichiosis, Tularemia)”, and 2) “Has anyone living on this residential property other than yourself, been diagnosed with a tick-borne disease (e.g., Lyme, Rocky Mountain Spotted Fever, Ehrlichiosis, Tularemia)”. All peri-domestic areas were sampled only once during the data collection period.
|Figure 1: Map of Indiana Counties, USA from which private residential properties were sampled|
Click here to view
First, we selected grids for sampling at each peri- domestic area, based on homeowner recommendation and density of vegetation. Tick density was standardized to 100m2 grid size of each peri-domestic area. All tick sampling procedures were performed on the selected grid. Ticks were sampled using a combination of Carbon dioxide (CO2) baiting and drag sampling,. Each peri-domestic area grid was dragged three times. All ticks found on the CO2 traps and drags were preserved in vials containing 70% ethyl alcohol, and returned to the lab for later identification. To minimize the potentially confounding effects of heavy dew and extreme heat on sampling efficiency, all tick sampling were performed on rain-free days, avoiding early morning and midday hours. Tick genus/species and life stages were identified morphologically under a stereomicroscope using standard taxonomic keys,,.
Ambient air temperature, relative humidity (RH), elevation, and coordinates of the sampling grid at each peri-domestic area were recorded at a height of 1-meter above ground level. Ambient air temperature and RH were recorded using a digital temperature humidity meter (Protmex MS6508). Elevation, coordinates and area of grid (meter squared) were obtained using a handheld Global Positioning System (GPS) (Garmin GPS eTrex® 30x) with a position accuracy of 3 meters. Soil moisture content (percentage relative saturation and pH readings were taken with a Kelway® Soil tester (Kel Instruments Co., Inc) which was inserted into the soil at the mid-point of the sampled grid. Other information recorded for each grid and peri-domestic area include prevailing weather condition (sunny vs. cloudy/overcast), grid description (shaded vs. grassy or mixed), time of day for sampling (evening vs. morning), property location (rural vs. urban), and leaf litter (presence vs. absence). Property location was designated as ‘rural’ if the peri-domestic area within a household’s property boundaries, and the neighborhood surrounding the yard consisted of 50% or more grassy/ wooded area, as indicated by the assessment of 2 different research assistants. The neighborhood as used in this study referred to all locations outside the peri-domestic area, but within 500 m of the peri-domestic boundary,. Otherwise, the private residential property was designated as ‘urban’.
For our tests of association, the primary outcome of interest was tick activity and density respectively. Research diagnostic criteria (RDC) for tick activity was the identification of at least one developmental stage (Larva, Nymph, or Adult) of any tick on the peri-domestic area. Tick density was defined as the total number of ticks sampled per 100m2 grid using CO2 trap and tick drag. We used 2 previously reported and a third criteria to determine established tick populations in a peri-domestic area. These were 1) identification of ≥; 6 ticks, OR 2) > 1 life stage, OR 3) two or more tick species. We included the third criteria for defining established tick populations, given that it fits well with the rationale for the first two criteria, that is, the presence of two or more tick species in a peri-domestic area is unlikely to constitute a transient tick sample.
We used frequency tabulation to determine self-reported peri-domestic TBD diagnosis (Yes/No), and proportion of peri-domestic areas with established tick populations. Peri-domestic areas with ≥ 6 ticks, or > 1 life stage, or > 1 tick species identified, were classified as having established tick populations, while peri-domestic areas that did not meet these criteria were classified as having reported tick populations. We used chi-square cross tabulation and paired t-testing to describe tick activity & density separately, by self-reported peri-domestic TBD. We used chi-square cross-tabulation and Fisher’s exact test to describe how tick activity (presence/absence) varied by study participants’ age group, gender, education, race, employment status, and County. We used the Altair package in Python to make a stacked bar graph of the tick density for the sampling period (June to November) stratified by species and life stage. Using Pearson’s correlation coefficient test we tested for correlation between mean tick density and microclimatic variables. Finally, we used log-binomial regression crude (unadjusted) models to estimate the prevalence ratios (PRs) for the associations between different covariates and tick presence/absence. The covariates modeled included soil moisture & pH levels, ambient air temperature, relative humidity, elevation (in feet), prevailing weather condition (sunny vs. cloudy/ overcast), grid description (shaded vs. grassy or mixed), time of day for sampling (evening vs. morning), property location (rural vs. urban), and leaf litter (presence vs. absence). All statistical analyses were conducted using RStudio version 1.1.414, and Python version 3.7.
| Results|| |
Self-reported peri-domestic TBD diagnosis (as indicated by number of individuals in the household who had previously been diagnosed with a TBD) was 16% (N = 15). However, we found no statistically significant association between self-reported peri-domestic TBD diagnosis and tick activity, X2 = 0.218 (df = 1, p = 0.6406). We also found no statistically significant difference in mean tick density by self-reported peri-domestic TBD diagnosis = 7.64, μ2 = 3.67; t = 0.508, df = 91, p-value = 0.6122).
Thirty-eight percent (N = 36) of peri-domestic areas sampled had tick activity, with a total count of 661 ticks. Of these, 50% (N = 18) had established tick populations, while the remaining fit our definition of reported tick populations. More ticks were sampled using drags (79%, N = 525) compared to CO2 traps (21.0%, N = 136). Across all species, nymphal ticks were the most predominant life stage sampled (68%, N = 452), followed by larval ticks (29%, N = 193), while adult ticks comprised only 2% (N = 16) [Table 1]. Amblyomma americanum (Linnaeus, 1758) was the most common tick specie sampled (67%, N = 444), followed by Dermacentor variabilis (Say, 1821) (30%, N = 198), while the remaining 3% (N = 19) were Ixodes scapularis (Say, 1821). On many peri-domestic areas more than one tick species was present.
|Table 1: Species and life stages of ticks found on peri-domestic areas in Indiana, USA|
Click here to view
Tick density was highest in August and lowest in November [Figure 2]. By life stage, I. scapularis was present from June to October, with nymphs occurring more than any other life stage across several months of sampling. Adult D. variabilis and nymph of A. americanum respectively occurred across several months of sampling (June – September) than any other life stage recorded within both species.
|Figure 2: Cumulative tick density by month (June to November) of sampling, species, and life stage in south-central Indiana peri-domestic areas|
Click here to view
We found no statistically significant differences in tick activity by homeowners’ gender, age category, race, education, employment status and income (see appendix table). However, the frequency of tick presence was more in the peri-domestic areas of study participants ≥ 45 years old. In log-binomial regression models, we found that for each unit increase in ambient air temperature, tick presence increased by 3% [PR (95% CI): 1.03 (1.01, 1.06)]. Compared to urban peri-domestic areas, rural properties were 2.07 times more likely to have tick presence [PR (95% CI): 2.07 (1.24, 3.44)]. Similarly, we found a positive correlation between tick density and ambient temperature [ρ, p-value): 0.2052, 0.0448]. In simple linear regression models, we found that for every unit increase in ambient temperature (in Fahrenheit) tick density increased by 0.42 [Coefficient estimate, p-value: 0.42, 0.0448]. Conversely, there was a significant negative correlation between tick density (density) and elevation [ρ, p-value: -0.255, 0.0122]. Specifically, for every foot increase in elevation, tick density decreased by 0.10 [Coefficient estimate, p-value: -0.10, 0.0122].
| Conclusion|| |
Our results reveal that thirty-eight percent of at-risk peri-domestic areas in south-central Indiana had tick activity. Of these, fifty-percent had established tick populations. Further, A. americanum tick was the most common tick in peri-domestic areas. Additionally, nymphal ticks were the most predominant life stage found on peri-domestic areas.
The prevalence of infection in nymphal life stage of ticks is generally used as the index of human risk of infection with TBD. The finding of more nymphal ticks than any other life stage in peri-domestic areas, coupled with the higher density of lonestar ticks would suggest a heightened risk of diseases transmitted by this tick species. Such diseases include Ehrlichiosis, Tularemia, Heartland virus, Bourbon virus, and Southern-tick associated rash illness (STARI). Additionally, the 50% of peri-domestic areas with established tick populations, may portend higher risk for tick exposure and tick-borne diseases in peri-domestic areas of south-central Indiana. Although, self-reported prevalence of peri-domestic tick-borne disease was sixteen-percent among study participants, we found no significant association between tick density and self-reported peri-domestic TBD diagnosis (even though the mean of the ‘Yes’ group [μ1 = 7.64] was nearly twice that of the ‘No’ group [μ2 = 3.67]. Nonetheless, previous studies have established high association between TBD incidence and tick density in peri-domestic areas across the U.S.,,,,,. It is quite possible that our current preliminary results are due to the limited sample size used in the current study remains rather than a true null association.
We found that increasing temperature is positively associated with tick activity. Raghavan, Goodin reported that temperature was predictive of A. americanum distribution in Kansas. Other studies have reported similar findings,,,. Given the positive association between increasing temperature and tick activity in this study, and the higher prevalence of A. americanum recorded, we expect a northward range expansion of A. americanum ticks which will be driven in part by climate change and increased environmental suitability. Finally, our study revealed that rural peri-domestic areas were significantly more likely to have tick activity, compared to urban property. Previous studies have shown that rural residential properties are more likely to be located in close proximity of grassy, forested woodland, with wildlife which serve as tick vertebrate hosts,,,,,,. Under such conditions, tick activity and density is expectedly high.
| Limitations|| |
The cross-sectional nature of our study means that we are unable to determine the temporal order of the associations tested in correlation and regression models. Additionally, seasonal variations in the distribution of various tick life stages have been known to occur. It is possible that the relative distribution of various tick life stages reported in this study could vary if repeat sampling was conducted at a different time/season of the year. The sample size is limited, and the results are preliminary. For these reasons our generalizations are limited in scope.
Despite these limitations, our preliminary study findings have important implications for active surveillance of ticks and for tick-borne disease risk reduction. Our results suggest that tick populations are established in many peri-domestic areas of south-central Indiana, and that tick density in peri-domestic areas is likely to be influenced by climate associated temperature rises. Furthermore, the predominance of nymphal stages of ticks in peri-domestic areas, is likely to increase infection risk for exposed populations. We also reported that rural peri-domestic areas had significantly more tick activity compared to urban peri-domestic areas.
Although these results are preliminary, they provide ample justification for active surveillance of tick distribution in Indiana, which is critical for targeting tick control and tick-borne disease prevention efforts. Other reasons for which continued tick surveillance is crucial include discovery of novel tick-borne pathogens in patients infected in peri-domestic areas,, and the role of seasonal migratory birds and other non-seasonal competent tick vertebrate hosts in peri-domestic areas in the propagation of tick-borne diseases,,,.
Given our study findings and the observed limitations, we suggest that future studies should investigate, 1) whether tick-borne diseases transmitted by A. americanum in Indiana are significantly associated with peri-domestic areas as place of tick exposure, 2) whether annual changes in temperature significantly affect tick distribution in Indiana, and 3) effects of tick vertebrate host diversity, different measures of tick control on tick distribution and tick-borne disease diagnosis in peri-domestic areas.
Conflict of interest: None
| Acknowledgements|| |
We gratefully acknowledge the support of all the homeowners in Indiana who willing provided sociodemographic data and permitted field sampling on the yard of their private residential property. Each participating homeowner received a USD 50 gift card for participation in this study. Study protocol was approved by the Human Subjects Office of Indiana University (IRB Protocol #: 1805516440).
| References|| |
Mead PS. Epidemiology of Lyme disease. Infectious Disease Clinics
Diuk-Wasser M, Gatewood A, Cortinas MR, Yaremych-Hamer S, Tsao J, Kitron U, et al
. Spatiotemporal patterns of host-seeking Ixodes scapularis nymphs (Acari: Ixodidae) in the United States. Journal of medical entomology
2014; 43(2): 166-76.
Stafford KC, Cartter ML, Magnarelli LA, Ertel S-H, Mshar PA. Temporal correlations between tick abundance and prevalence of ticks infected with Borrelia burgdorferi and increasing incidence of Lyme disease. Journal of clinical microbiology
Donohoe H, Omodior O, Roe J. Tick-borne disease occupational risks and behaviors of Florida Fish, Wildlife, and Parks Service employees–a health belief model perspective. Journal of outdoor recreation and tourism
2018; 22: 9-17.
Omodior O, Pennington-Gray L, Donohoe H. Efficacy of the Theory of Planned Behavior in Predicting the Intention to Engage in Tick-Borne Disease Personal Protective Behavior Amongst Visitors to an Outdoor Recreation Center. Journal of Park and Recreation Administration
Fischhoff IR, Bowden SE, Keesing F, Ostfeld RS. Systematic review and meta-analysis of tick-borne disease risk factors in residential yards, neighborhoods, and beyond. BMC infectious diseases
Kilpatrick HJ, Labonte AM, Stafford III KC. The relationship between deer density, tick abundance, and human cases of Lyme disease in a residential community. Journal of Medical Entomology
Omodior O, Kianersi S, Luetke M. Spatial Clusters and Non-spatial Predictors of Tick-Borne Disease Diagnosis in Indiana. Journal of community health
2019; 44(6): 1111-1119
Omodior O, Kianersi S, Luetke M. Prevalence of Risk and Protective Factors for Tick Exposure and Tick-Borne Disease Among Residents of Indiana. Journal of public health management and practice:
Wallace D, Ratti V, Kodali A, Winter JM, Ayres MP, Chipman JW, et al
. Effect of Rising Temperature on Lyme Disease: Ixodes scapularis Population Dynamics and Borrelia burgdorferi Transmission and Prevalence. Journal canadien des maladies infectieuses et de la microbiologie medicale
. 2019; 9817930.
Eisen RJ, Eisen L, Ogden NH, Beard CB. Linkages of Weather and Climate With Ixodes scapularis and Ixodes pacificus (Acari: Ixodidae), Enzootic Transmission of Borrelia burgdorferi, and Lyme Disease in North America. J Med Entomol
2016; 53(2): 250-61.
MacDonald AJ, Hyon DW, Brewington JB, 3rd, O’Connor KE, Swei A, Briggs CJ. Lyme disease risk in southern California: abiotic and environmental drivers of Ixodes pacificus (Acari: Ixodidae) density and infection prevalence with Borrelia burgdorferi. Parasit Vectors
2017; 10(1): 7.
Biernacki P, Waldorf D. Snowball sampling: Problems and techniques of chain referral sampling. Sociological methods & research
1981; 10(2): 141-63.
Connally NP, Ginsberg HS, Mather TN. Assessing peridomestic entomological factors as predictors for Lyme disease. Journal of Vector Ecology
2006; 31(2): 364-70.
Spickett AM, Van Ark H. Drag-sampling of free-living ixodid ticks in the Kruger National Park. Onderstepoort J Vet Res
199; 58(1): 27-32.
Wilson JG, Kinzer DR, Sauer JR, Hair JA. Chemo-attraction in the lone star tick (Acarina: Ixodidae): I. Response of different developmental stages to carbon dioxide administered via traps. Journal of Medical Entomology
1972; 9(3): 245-52.
Diuk-Wasser M, Gatewood A, Cortinas MR, Yaremych-Hamer S, Tsao J, Kitron U, et al
. Spatiotemporal patterns of host-seeking Ixodes scapularis nymphs (Acari: Ixodidae) in the United States. Journal of medical entomology
2006; 43(2): 166-76.
Keirans JE, Litwak TR. Pictorial key to the adults of hard ticks, family Ixodidae (Ixodida: Ixodoidea), east of the Mississippi River. Journal of Medical Entomology
1989; 26(5): 435-48.
Keirans JE, Durden LA. Illustrated key to nymphs of the tick genus Amblyomma (Acari: Ixodidae) found in the United States. Journal of Medical Entomology
1998; 35(4): 489-95.
Clifford CM, Anastos G. The use of chaetotaxy in the identification of larval ticks (Acarina: Ixodidae). The Journal of Parasitology
1960; 46(5): 567-78.
Hasanzadeh K, Broberg A, Kyttä M. Where is my neighborhood? A dynamic individual-based definition of home ranges and implementation of multiple evaluation criteria. Applied geography
Dennis DT, Nekomoto TS, Victor JC, Paul WS, Piesman J. Reported distribution of Ixodes scapularis and Ixodes pacificus (Acari: Ixodidae) in the United States. Journal of medical entomology
1998; 35(5): 629-38.
LoGiudice K, Ostfeld RS, Schmidt KA, Keesing F. The ecology of infectious disease: Effects of host diversity and community composition on Lyme disease risk. Proceedings of the National Academy of Sciences
2003; 100(2): 567-71.
Molloy PJ, Telford SR, Chowdri HR, Lepore TJ, Gugliotta JL, Weeks KE, et al
. Borrelia miyamotoi disease in the northeastern United States: a case series. Annals of internal medicine
. 2015; 163(2): 91-8.
Christensen J, Fischer RJ, McCoy BN, Raffel SJ, Schwan TG. Tickborne relapsing fever, Bitterroot Valley, Montana, USA. Emerging infectious diseases
2015; 21(2): 217.
Stafford III KC. Tick management handbook. An integrated guide for homeowners, pest control operators and public health officials for the prevention of tick-associated diseases New Haven, USA: The Connecticut Agricultural Experiment Station. 2004.
Steere AC, Malawista SE, Snydman DR, Shope RE, Andiman WA, Ross MR, et al
. An epidemic of oligoarticular arthritis in children and adults in three Connecticut communities. Arthritis & Rheumatism. Official Journal of the American College of Rheumatology
1977; 20(1): 7-17.
Mast WE, Burrows WM. Erythema chronicum migrans in the United States. JAMA
1976; 236(7): 859-60.
Falco RC, Fish D. Prevalence of Ixodes dammini near the homes of Lyme disease patients in Westchester County, New York. American Journal of Epidemiology
Raghavan RK, Goodin DG, Hanzlicek GA, Zolnerowich G, Dryden MW, Anderson GA, et al. Maximum entropy-based ecological niche model and bio-climatic determinants of Lone Star tick (Amblyomma americanum) niche. Vector-Borne and Zoonotic Diseases
2016; 16(3): 205-11.
Schwartz BS, Goldstein MD. Lyme disease in outdoor workers: risk factors, preventive measures, and tick removal methods. American Journal of Epidemiology
Glass GE, Schwartz BS, Morgan III JM, Johnson DT, Noy PM, Israel E. Environmental risk factors for Lyme disease identified with geographic information systems. American journal of public health
1995; 85(7): 944-8.
Schulze TL, Taylor RC, Taylor GC, Bosler EM. Lyme disease: a proposed ecological index to assess areas of risk in the northeastern United States. American journal of public health
Carey AB, Krinsky WL, Main AJ. Ixodes dammini (Acari: Ixodidae) and associated ixodid ticks in south-central Connecticut, USA. Journal of Medical Entomology
Kowalczyk JP, Smith TL. Bird Feeders and the Spatial Distribution of Ticks on a Residential Lawn in Worcester County, Massachusetts. Northeastern Naturalist
Hamer S, Lehrer E, Magle S. Wild birds as sentinels for multiple zoonotic pathogens along an urban to rural gradient in greater Chicago, Illinois. Zoonoses and Public Health
2012; 59(5): 355-64.
Richter D, Spielman A, Komar N, Matuschka F-R. Competence of American robins as reservoir hosts for Lyme disease spirochetes. Emerging infectious diseases
2000; 6(2): 133.
[Figure 1], [Figure 2]