Sarah A. Hamer

Human risk of infection with Borrelia burgdorferi, the Lyme disease agent, in eastern United States.

The geographic pattern of human risk for infection with Borrelia burgdorferi sensu stricto, the tick-borne pathogen that causes Lyme disease, was mapped for the eastern United States. The map is based on standardized field sampling in 304 sites of the density of Ixodes scapularis host-seeking nymphs infected with B. burgdorferi, which is closely associated with human infection risk. Risk factors for the presence and density of infected nymphs were used to model a continuous 8 km×8 km resolution predictive surface of human risk, including confidence intervals for each pixel. Discontinuous Lyme disease risk foci were identified in the Northeast and upper Midwest, with a transitional zone including sites with uninfected I. scapularis populations. Given frequent under- and over-diagnoses of Lyme disease, this map could act as a tool to guide surveillance, control, and prevention efforts and act as a baseline for studies tracking the spread of infection.

Climate and tick seasonality are predictors of Borrelia burgdorferi genotype distribution.

ABSTRACT The blacklegged tick, Ixodes scapularis, is of significant public health importance as a vector of Borrelia burgdorferi, the agent of Lyme borreliosis. The timing of seasonal activity of each immature I. scapularis life stage relative to the next is critical for the maintenance of B. burgdorferi because larvae must feed after an infected nymph to efficiently acquire the infection from reservoir hosts. Recent studies have shown that some strains of B. burgdorferi do not persist in the primary reservoir host for more than a few weeks, thereby shortening the window of opportunity between nymphal and larval feeding that sustains their enzootic maintenance. We tested the hypothesis that climate is predictive of geographic variation in the seasonal activity of I. scapularis, which in turn differentially influences the distribution of B. burgdorferi genotypes within the geographic range of I. scapularis. We analyzed the relationships between climate, seasonal activity of I. scapularis, and B. burgdorferi genotype frequency in 30 geographically diverse sites in the northeastern and midwestern United States. We found that the magnitude of the difference between summer and winter daily temperature maximums was positively correlated with the degree of seasonal synchrony of the two immature stages of I. scapularis. Genotyping revealed an enrichment of 16S-23S rRNA intergenic spacer restriction fragment length polymorphism sequence type 1 strains relative to others at sites with lower seasonal synchrony. We conclude that climate-associated variability in the timing of I. scapularis host seeking contributes to geographic heterogeneities in the frequencies of B. burgdorferi genotypes, with potential consequences for Lyme borreliosis morbidity.

Geographic Variation in the Relationship between Human Lyme Disease Incidence and Density of Infected Host-Seeking Ixodes scapularis Nymphs in the Eastern United States

Prevention and control of Lyme disease is difficult because of the complex biology of the pathogens (Borrelia burgdorferi) vector (Ixodes scapularis) and multiple reservoir hosts with varying degrees of competence. Cost-effective implementation of tick- and host-targeted control methods requires an understanding of the relationship between pathogen prevalence in nymphs, nymph abundance, and incidence of human cases of Lyme disease. We quantified the relationship between estimated acarological risk and human incidence using county-level human case data and nymphal prevalence data from field-derived estimates in 36 eastern states. The estimated density of infected nymphs (mDIN) was significantly correlated with human incidence (r = 0.69). The relationship was strongest in high-prevalence areas, but it varied by region and state, partly because of the distribution of B. burgdorferi genotypes. More information is needed in several high-prevalence states before DIN can be used for cost-effectiveness analyses.

Wild Birds and Urban Ecology of Ticks and Tick-borne Pathogens, Chicago, Illinois, USA, 2005-2010

No longer do you have to visit rural areas to find ticks; birds are flying them directly to you. When researchers sampled several thousand birds in Chicago, they found that some carried ticks and that some of these ticks carried the organism that spreads Lyme disease. Although the number of infected ticks on these birds was low, risk for their invading an area and spreading infection to humans cannot be ignored. If conditions are favorable, a few infected ticks can quickly multiply. Migratory birds also carried tick species only known to be established in Central and South America. Limited introduction and successful establishment of ticks and disease-carrying organisms pose a major health risk for humans, wildlife, and domestic animals in urban environments worldwide.

Use of tick surveys and serosurveys to evaluate pet dogs as a sentinel species for emerging Lyme disease.

OBJECTIVE To evaluate dogs as a sentinel species for emergence of Lyme disease in a region undergoing invasion by Ixodes scapularis. SAMPLE POPULATION 353 serum samples and 78 ticks obtained from dogs brought to 18 veterinary clinics located in the lower peninsula of Michigan from July 15, 2005, through August 15, 2005. PROCEDURES Serum samples were evaluated for specific antibodies against Borrelia burgdorferi by use of 3 serologic assays. Ticks from dogs were subjected to PCR assays for detection of pathogens. RESULTS Of 353 serum samples from dogs in 18 counties in 2005, only 2 (0.6%) contained western blot analysis-confirmed antibodies against B burgdorferi. Ten of 13 dogs with I scapularis were from clinics within or immediately adjacent to the known tick invasion zone. Six of 18 I scapularis and 12 of 60 noncompetent vector ticks were infected with B burgdorferi. No ticks were infected with Anaplasma phagocytophilum, and 3 were infected with Babesia spp. CONCLUSIONS AND CLINICAL RELEVANCE Serosurvey in dogs was found to be ineffective in tracking early invasion dynamics of I scapularis in this area. Tick chemoprophylaxis likely reduces serosurvey sensitivity in dogs. Ticks infected with B burgdorferi were more common and widely dispersed than seropositive dogs. In areas of low tick density, use of dogs as a source of ticks is preferable to serosurvey for surveillance of emerging Lyme disease. IMPACT FOR HUMAN MEDICINE By retaining ticks from dogs for identification and pathogen testing, veterinarians can play an important role in early detection in areas with increasing risk of Lyme disease.

Wild Birds as Sentinels for Multiple Zoonotic Pathogens Along an Urban to Rural Gradient in Greater Chicago, Illinois

Wild birds are important in the maintenance and transmission of many zoonotic pathogens. With increasing urbanization and the resulting emergence of zoonotic diseases, it is critical to understand the relationships among birds, vectors, zoonotic pathogens, and the urban landscape. Here, we use wild birds as sentinels across a gradient of urbanization to understand the relative risk of diseases caused by three types of zoonotic pathogens: Salmonella pathogens, mosquito‐borne West Nile virus (WNV) and tick‐borne pathogens, including the agents of Lyme disease and human anaplasmosis. Wild birds were captured using mist nets at five sites throughout greater Chicago, Illinois, and blood, faecal and ectoparasite samples were collected for diagnostic testing. A total of 289 birds were captured across all sites. A total of 2.8% of birds harboured Ixodes scapularis– the blacklegged tick – of which 54.5% were infected with the agent of Lyme disease, and none were infected with the agent of human anaplasmosis. All infested birds were from a single site that was relatively less urban. A single bird, captured at the only field site in which supplemental bird feeding was practised within the mist netting zone, was infected with Salmonella enterica subspecies enterica. While no birds harboured WNV in their blood, 3.5% of birds were seropositive, and birds from more urban sites had higher exposure to the virus than those from less urban sites. Our results demonstrate the presence of multiple bird‐borne zoonotic pathogens across a gradient of urbanization and provide an assessment of potential public health risks to the high‐density human populations within the area.

Diverse Borrelia burgdorferi Strains in a Bird-Tick Cryptic Cycle†

ABSTRACT The blacklegged tick Ixodes scapularis is the primary vector of the most prevalent vector-borne zoonosis in North America, Lyme disease (LD). Enzootic maintenance of the pathogen Borrelia burgdorferi by I. scapularis and small mammals is well documented, whereas its “cryptic” maintenance by other specialist ticks and wildlife hosts remains largely unexplored because these ticks rarely bite humans. We quantified B. burgdorferi infection in a cryptic bird-rabbit-tick cycle. Furthermore, we explored the role of birds in maintaining and moving B. burgdorferi strains by comparing their genetic diversity in this cryptic cycle to that found in cycles vectored by I. scapularis. We examined birds, rabbits, and small mammals for ticks and infection over a 4-year period at a focal site in Michigan, 90 km east of a zone of I. scapularis invasion. We mist netted 19,631 birds that yielded 12,301 ticks, of which 86% were I. dentatus, a bird-rabbit specialist. No resident wildlife harbored I. scapularis, and yet 3.5% of bird-derived ticks, 3.6% of rabbit-derived ticks, and 20% of rabbit ear biopsy specimens were infected with B. burgdorferi. We identified 25 closely related B. burgdorferi strains using an rRNA gene intergenic spacer marker, the majority (68%) of which had not been reported previously. The presence of strains common to both cryptic and endemic cycles strongly implies bird-mediated dispersal. Given continued large-scale expansion of I. scapularis populations, we predict that its invasion into zones of cryptic transmission will allow for bridging of novel pathogen strains to humans and animals.

Shelter dogs as sentinels for Trypanosoma cruzi transmission across Texas.

Chagas disease, an infection with the parasite Trypanosoma cruzi, is increasingly diagnosed among humans in the southern United States. We assessed exposure of shelter dogs in Texas to T. cruzi; seroprevalence across diverse ecoregions was 8.8%. Canine serosurveillance is a useful tool for public health risk assessment.

Associations of passerine birds, rabbits, and ticks with Borrelia miyamotoi and Borrelia andersonii in Michigan, U.S.A.

BackgroundWild birds contribute to maintenance and dissemination of vectors and microbes, including those that impact human, domestic animal, and wildlife health. Here we elucidate roles of wild passerine birds, eastern cottontail rabbits (Sylvilagus floridanus), and Ixodes dentatus ticks in enzootic cycles of two spirochetes, Borrelia miyamotoi and B. andersonii in a region of Michigan where the zoonotic pathogen B. burgdorferi co-circulates.MethodsOver a four-year period, wild birds (n = 19,631) and rabbits (n = 20) were inspected for tick presence and ear tissue was obtained from rabbits. Samples were tested for Borrelia spirochetes using nested PCR of the 16S-23S rRNA intergenic spacer region (IGS) and bidirectional DNA sequencing. Natural xenodiagnosis was used to implicate wildlife reservoirs.ResultsIxodes dentatus, a tick that specializes on birds and rabbits and rarely bites humans, was the most common tick found, comprising 86.5% of the 12,432 ticks collected in the study. The relapsing fever group spirochete B. miyamotoi was documented for the first time in ticks removed from wild birds (0.7% minimum infection prevalence; MIP, in I. dentatus), and included two IGS strains. The majority of B. miyamotoi-positive ticks were removed from Northern Cardinals (Cardinalis cardinalis). Borrelia andersonii infected ticks removed from birds (1.6% MIP), ticks removed from rabbits (5.3% MIP), and rabbit ear biopsies (5%) comprised twelve novel IGS strains. Six species of wild birds were implicated as reservoirs for B. andersonii. Frequency of I. dentatus larval and nymphal co-feeding on birds was ten times greater than expected by chance. The relatively well-studied ecology of I. scapularis and the Lyme disease pathogen provides a context for understanding how the phenology of bird ticks may impact B. miyamotoi and B. andersonii prevalence and host associations.ConclusionsGiven the current invasion of I. scapularis, a human biting species that serves as a bridge vector for Borrelia spirochetes, human exposure to B. miyamotoi and B. andersonii in this region may increase. The presence of these spirochetes underscores the ecological complexity within which Borrelia organisms are maintained and the need for diagnostic tests to differentiate among these organisms.

Combining Public Health Education and Disease Ecology Research: Using Citizen Science to Assess Chagas Disease Entomological Risk in Texas.

Background Chagas disease is a zoonotic parasitic disease well-documented throughout the Americas and transmitted primarily by triatomine ‘kissing bug’ vectors. In acknowledgment of the successful history of vector control programs based on community participation across Latin America, we used a citizen science approach to gain novel insight into the geographic distribution, seasonal activity, and Trypanosoma cruzi infection prevalence of kissing bugs in Texas while empowering the public with information about Chagas disease. Methodology/Principal Findings We accepted submissions of kissing bugs encountered by the public in Texas and other states from 2013–2014 while providing educational literature about Chagas disease. In the laboratory, kissing bugs were identified to species, dissected, and tested for T. cruzi infection. A total of 1,980 triatomines were submitted to the program comprised of at least seven species, of which T. gerstaeckeri and T. sanguisuga were the most abundant (85.7% of submissions). Triatomines were most commonly collected from dog kennels and outdoor patios; Overall, 10.5% of triatomines were collected from inside the home. Triatomines were submitted from across Texas, including many counties which were not previously known to harbor kissing bugs. Kissing bugs were captured primarily throughout April-October, and peak activity occurred in June-July. Emails to our dedicated account regarding kissing bugs were more frequent in the summer months (June-August) than the rest of the year. We detected T. cruzi in 63.3% of tested bugs. Conclusions/Significance Citizen science is an efficient approach for generating data on the distribution, phenology, and infection prevalence of kissing bugs—vectors of the Chagas disease parasite—while educating the public and medical community.