Emerging patterns in rodent-borne zoonotic diseases.

Rodents are ubiquitous and typically unwelcome dwellers in human habitats worldwide, infesting homes, farm fields, and agricultural stores and potentially shedding disease-causing microbes into the most human-occupied of spaces. Of the vertebrate animal taxa that share pathogens with us, rodents are the most abundant and diverse, with hundreds of species of confirmed zoonotic hosts, some of which have nearly global distributions. However, only 12% of rodent species are known to be sources of pathogens that also infect people, and those rodents that do are now recognized as tending to share a suite of predictable traits. Here, we characterize those traits and explore them in the context of three emerging or reemerging rodent-borne zoonotic diseases of people: Lassa fever, Lyme disease, and plague.

Hitchhiker's Guide to Borrelia burgdorferi.

Don't Panic. In the nearly 50 years since the discovery of Lyme disease, Borrelia burgdorferi has emerged as an unlikely workhorse of microbiology. Interest in studying host-pathogen interactions fueled significant progress in making the fastidious microbe approachable in laboratory settings, including the development of culture methods, animal models, and genetic tools. By developing these systems, insight has been gained into how the microbe is able to survive its enzootic cycle and cause human disease. Here, we discuss the discovery of B. burgdorferi and its development as a model organism before diving into the critical lessons we have learned about B. burgdorferi biology at pivotal stages of its lifecycle: gene expression changes during the tick blood meal, colonization of a new vertebrate host, and developing a long-lasting infection in that vertebrate until a new tick feeds. Our goal is to highlight the advancements that have facilitated B. burgdorferi research and identify gaps in our current understanding of the microbe.

Mouse Models for the Study of Borrelia burgdorferi Infection.

Lyme disease, a tickborne illness caused by Borrelia burgdorferi, is an emerging, significant public health concern. B. burgdorferi infections are challenging to study because of their complex life cycle that requires adaptation to both ticks and mammalian hosts for long-term survival and transmission. Bacterial adaptation is accomplished through extensive gene expression alterations in response to environmental cues that remain to be more fully explored. Mouse models of infection serve as valuable tools for studying B. burgdorferi adaptation to the mammalian host and the spirochete's ability to cause persistent infections and thus to interact with and evade the immune system. This article details three mouse models that differ in their primary methods of infection: infestation with B. burgdorferi infected ticks, intradermal inoculation of culture-grown spirochetes, and infection via subcutaneous transplantation of infected tissue. Each method offers unique advantages and limitations. Tick infestation is the route of natural transmission but presents logistical challenges. Syringe inoculation is easy and provides precise control over the infectious dose, but infection is with culture-adapted bacteria. Transplantation of infected tissue introduces mammalian-host-adapted B. burgdorferi in precise anatomical locations, but misses the transfer of tick factors affecting immunity. Detailed protocols are provided for each of the three infection routes, and pros and cons of each method are outlined to help researchers identify the best approach for a research question to be addressed. A protocol is also provided for the treatment of mice with antibiotics that reliably eliminates detectable spirochetes from the animals. © 2024 Wiley Periodicals LLC. Basic Protocol 1: Syringe inoculation of mice with cultured B. burgdorferi and collection of necropsy tissues Basic Protocol 2: Infection of mice with B. burgdorferi via tick infestation Basic Protocol 3: Infection of mice with host-adapted B. burgdorferi via tissue transplant Support Protocol: Clearance of B. burgdorferi by antibiotic treatment.

The effect of fluralaner treatment of small mammals on the endemic cycle of Borrelia burgdorferi in a natural environment.

Among approaches aimed at reducing Lyme disease risk in the environment, those targeting reservoirs of Borrelia burgdorferi Johnson are promising because they have the potential to reduce both the density of questing Ixodes scapularis Say (Acari: Ixodidea) ticks and the prevalence of B. burgdorferi in the tick population. In this 4-yr field study, we treated a population of wild small mammals with 2 densities of fluralaner baits and investigated the effect of the treatment on 3 parameters of the endemic cycle of B. burgdorferi: (i) the prevalence of infected Peromyscus mice (PIM), (ii) the density of questing nymphs (DON), and (iii) the prevalence of infected questing nymphs (NIP). We demonstrated that fluralaner baiting is effective at reducing tick infestation of Peromyscus mice, the main reservoir of B. burgdorferi in central and northeastern North America, in the laboratory and the field. Results from this study showed a significant decrease in B. burgdorferi infection in mice (odds ratio: 0.37 [CI95: 0.17 to 0.83]). A reduction in the DON between 45.4% [CI95: 22.4 to 61.6] and 62.7% [CI95: 45.9 to 74.2] occurred in treated area when compared with control areas. No significant effect was reported on the NIP. These results confirm the hypothesis that fluralaner baits have an effect on B. burgdorferi endemic cycle, with the potential to reduce the density of B. burgdorferi-infected ticks in the environment. Further studies performed in various habitats and public health intervention contexts are needed to refine and operationalize this approach for reducing Lyme disease risk in the environment.

Natural selection and recombination at host-interacting lipoprotein loci drive genome diversification of Lyme disease and related bacteria.

Lyme disease, caused by spirochetes in the Borrelia burgdorferi sensu lato clade within the Borrelia genus, is transmitted by Ixodes ticks and is currently the most prevalent and rapidly expanding tick-borne disease in Europe and North America. We report complete genome sequences of 47 isolates that encompass all established species in this clade while highlighting the diversity of the widespread human pathogenic species B. burgdorferi. A similar set of plasmids has been maintained throughout Borrelia divergence, indicating that they are a key adaptive feature of this genus. Phylogenetic reconstruction of all sequenced Borrelia genomes revealed the original divergence of Eurasian and North American lineages and subsequent dispersals that introduced B. garinii, B. bavariensis, B. lusitaniae, B. valaisiana, and B. afzelii from East Asia to Europe and B. burgdorferi and B. finlandensis from North America to Europe. Molecular phylogenies of the universally present core replicons (chromosome and cp26 and lp54 plasmids) are highly consistent, revealing a strong clonal structure. Nonetheless, numerous inconsistencies between the genome and gene phylogenies indicate species dispersal, genetic exchanges, and rapid sequence evolution at plasmid-borne loci, including key host-interacting lipoprotein genes. While localized recombination occurs uniformly on the main chromosome at a rate comparable to mutation, lipoprotein-encoding loci are recombination hotspots on the plasmids, suggesting adaptive maintenance of recombinant alleles at loci directly interacting with the host. We conclude that within- and between-species recombination facilitates adaptive sequence evolution of host-interacting lipoprotein loci and contributes to human virulence despite a genome-wide clonal structure of its natural populations. IMPORTANCE: Lyme disease (also called Lyme borreliosis in Europe), a condition caused by spirochete bacteria of the genus Borrelia, transmitted by hard-bodied Ixodes ticks, is currently the most prevalent and rapidly expanding tick-borne disease in the United States and Europe. Borrelia interspecies and intraspecies genome comparisons of Lyme disease-related bacteria are essential to reconstruct their evolutionary origins, track epidemiological spread, identify molecular mechanisms of human pathogenicity, and design molecular and ecological approaches to disease prevention, diagnosis, and treatment. These Lyme disease-associated bacteria harbor complex genomes that encode many genes that do not have homologs in other organisms and are distributed across multiple linear and circular plasmids. The functional significance of most of the plasmid-borne genes and the multipartite genome organization itself remains unknown. Here we sequenced, assembled, and analyzed whole genomes of 47 Borrelia isolates from around the world, including multiple isolates of the human pathogenic species. Our analysis elucidates the evolutionary origins, historical migration, and sources of genomic variability of these clinically important pathogens. We have developed web-based software tools (BorreliaBase.org) to facilitate dissemination and continued comparative analysis of Borrelia genomes to identify determinants of human pathogenicity.

An Updated Review on the Spatial Distribution of Borrelia burgdorferi Sensu Lato Across Ticks, Animals and Humans in Northeastern China and Adjacent Regions.

BACKGROUND: Lyme disease is a tick-borne zoonotic disease caused by Borrelia burgdorferi sensu lato and is prevalent in northeastern Asia, particularly in the forested area of Northeastern China. However, a lack of systematic data on the spatial distribution of B. burgdorferi in this region hinders the prediction of its transmission risk across the landscape. METHODS: To provide an updated overview and establish a comprehensive spatial distribution database, we conducted a systematic review of literature published between 2000 and 2022. We collected and compiled relevant data on B. burgdorferi in Northeastern China and its neighbouring regions, outlining its distribution in ticks, wild animals, livestock and humans. Spatial analysis was performed to identify spatial clusters of tick positivity and host infection rates. RESULTS: From a total of 1823 literature, we selected 110 references to compile 626 detection records of B. burgdorferi, including 288 in ticks, 109 in wildlife, 111 in livestock and domestic animals and 100 in humans. The average detection rate of B. burgdorferi in ticks was approximately 20%, with wildlife, livestock and domestic animal host positivity rates below 50% and human seroprevalence rates varying from 0.94% to 44.18%. CONCLUSIONS: The study identified the presence of 17 tick species and ten genotypes of B. burgdorferi in the region, indicating a broad distribution. Notably, B. burgdorferi exhibited notable clustering, particularly in the central and eastern areas of Jilin Province, warranting further investigation.

Host-pathogen associations inferred from bloodmeal analyses of Ixodes scapularis ticks in a low biodiversity setting.

Tick-borne pathogen emergence is dependent on the abundance and distribution of competent hosts in the environment. Ixodes scapularis ticks are generalist feeders, and their pathogen infection prevalence depends on their relative feeding on local competent and non-competent hosts. The ability to determine what host a larval life stage tick fed on can help predict infection prevalence, emergence, and spread of certain tick-borne pathogens and the risks posed to public health. Here, we use a newly developed genomic target-based technique to detect the source of larval bloodmeals by sampling questing nymphs from Block Island, RI, a small island with a depauperate mammalian community. We used previously designed specific assays to target all known hosts on this island and analyzed ticks for four human pathogenic tick-borne pathogens. We determined the highest proportion of larvae fed on avian species (42.34%), white-footed mice (36.94%), and white-tailed deer (20.72%) and occasionally fed on feral cats, rats, and voles, which are in low abundance on Block Island. Additionally, larvae that had fed on white-footed mice were significantly more likely to be infected with Borrelia burgdorferi and Babesia microti, while larvae that had fed on white-footed mice or white-tailed deer were significantly more likely to be infected with, respectively, mouse- and deer-associated genotypes of Anaplasma phagocytophilum. The ability to detect a nymph's larval host allows for a better understanding of tick feeding behavior, host distribution, pathogen prevalence, and zoonotic risks to humans, which can contribute to better tick management strategies. IMPORTANCE: Tick-borne diseases, such as Lyme disease, babesiosis, and anaplasmosis, pose significant public health burdens. Tick bloodmeal analysis provides a noninvasive sampling method to evaluate tick-host associations and combined with a zoonotic pathogen assay, can generate crucial insights into the epidemiology and transmission of tick-borne diseases by identifying potential key maintenance hosts. We investigated the bloodmeals of questing Ixodes scapularis nymphs. We found that avian hosts, white-footed mice, and white-tailed deer fed the majority of larval ticks and differentially contributed to the prevalence of multiple tick-borne pathogens and pathogen genotypes in a low biodiversity island setting. Unraveling the intricate network of host-vector-pathogen interactions will contribute to improving wildlife management and conservation efforts, to developing targeted surveillance, and vector and host control efforts, ultimately reducing the incidence of tick-borne diseases and improving public health.

Modeling platform to assess the effectiveness of single and integrated Ixodes scapularis tick control methods.

BACKGROUND: Lyme disease continues to expand in Canada and the USA and no single intervention is likely to curb the epidemic. METHODS: We propose a platform to quantitatively assess the effectiveness of a subset of Ixodes scapularis tick management approaches. The platform allows us to assess the impact of different control treatments, conducted either individually (single interventions) or in combination (combined efforts), with varying timings and durations. Interventions include three low environmental toxicity measures in differing combinations, namely reductions in white-tailed deer (Odocoileus virginianus) populations, broadcast area-application of the entomopathogenic fungus Metarhizium anisopliae, and fipronil-based rodent-targeted bait boxes. To assess the impact of these control efforts, we calibrated a process-based mathematical model to data collected from residential properties in the town of Redding, southwestern Connecticut, where an integrated tick management program to reduce I.xodes scapularis nymphs was conducted from 2013 through 2016. We estimated parameters mechanistically for each of the three treatments, simulated multiple combinations and timings of interventions, and computed the resulting percent reduction of the nymphal peak and of the area under the phenology curve. RESULTS: Simulation outputs suggest that the three-treatment combination and the bait boxes-deer reduction combination had the overall highest impacts on suppressing I. scapularis nymphs. All (single or combined) interventions were more efficacious when implemented for a higher number of years. When implemented for at least 4 years, most interventions (except the single application of the entomopathogenic fungus) were predicted to strongly reduce the nymphal peak compared with the no intervention scenario. Finally, we determined the optimal period to apply the entomopathogenic fungus in residential yards, depending on the number of applications. CONCLUSIONS: Computer simulation is a powerful tool to identify the optimal deployment of individual and combined tick management approaches, which can synergistically contribute to short-to-long-term, costeffective, and sustainable control of tick-borne diseases in integrated tick management (ITM) interventions.

Contrasting Perceptions, Knowledge, and Actions around Lyme Disease in an Urban Area of Emerging Lyme Disease and an Area of Endemic Lyme Disease in the Northeastern United States.

Lyme disease transmission dynamics in the northeastern United States vary by context. Periurban regions, including Block Island, RI, have experienced decades of endemic transmission. In urban areas, including Staten Island, a borough in New York City, NY, Lyme disease is an emerging issue. Knowledge, attitudes, and practices around Lyme disease evolve as an area progresses from emergent to endemic. We conducted focus group discussions and household surveys within Staten Island, NY and Block Island, RI to compare knowledge, attitudes, and practices surrounding Lyme disease and other tick-borne diseases. Qualitative data were coded into themes, and survey data were used to provide more general context of the focus group discussions. Using item response theory, we developed an index of knowledge from relevant factors within the household survey. We identified a significant difference in knowledge scores between the two study areas. Additionally, we identified key differences across multiple domains. Participants from Block Island were more likely to report prior tick exposure and Lyme disease in themselves or household members and were more likely to express concerns about the environmental impact of mitigation strategies. Individuals on Staten Island were more likely to assign responsibility of prevention and control to local, state, and federal government than to take personal prevention measures. Prevention of Lyme disease and other tick-borne diseases must be tailored to the community context and monitored over time as perceptions and priorities may evolve as transmission dynamics transition from emergent to endemic.

Outdoor worker knowledge of ticks and Lyme disease in Québec.

BACKGROUND AND AIMS: Lyme disease is a well-known occupational risk across North America caused by exposure to Borrelia burgdorferi via blacklegged ticks (Ixodes scapularis). As the geographic range of B. burgdorferi advances with the increasing distribution of blacklegged ticks, more outdoor workers are at risk of contracting Lyme disease. In this study, we examined the demography and personal perceptions of outdoor workers within one framework to better determine the overall risk for those working outdoors. METHODS AND RESULTS: We analysed outdoor worker knowledge of ticks and of behaviours that can prevent tick bites and Lyme disease. We then compared these risk perceptions of individuals across age, sex, education, and industry, as well as time spent outdoors. We tested the hypothesis that the risk perception of an individual and their knowledge of Lyme disease transmission was dependent on their demographics, experience in their job, and the region in which they spend time outdoors. We estimated a knowledge-based risk score based on individuals' answers to a questionnaire on risk perception given to voluntary participants who work outdoors. Those who had higher risk scores were more at risk. We found that knowledge-based risk scores were correlated with geographic risk levels and with the number of hours per day spent outdoors. Those who work longer hours and who work in areas with mid-level risk had higher risk scores. Those who spend more time outdoors recreationally had lower risk scores. CONCLUSIONS: Further examination and acknowledgment of the reasoning behind why these factors are affecting workers' risks must be considered to recognize that it is not necessarily demographics or geographically high-risk areas that affect an individual's risk. Workers' knowledge of these risks is affected by several variables that should be taken into consideration when implementing safety measures and awareness programs.

Population dynamics of the Lyme disease bacterium, Borrelia burgdorferi, during rapid range expansion in New York State.

Recent changes in climate and human land-use have resulted in alterations of the geographic range of many species, including human pathogens. Geographic range expansion and population growth of human pathogens increase human disease risk. Relatively little empirical work has investigated the impact of range changes on within-population variability, a contributor to both colonization success and adaptive potential, during the precise time in which populations are colonized. This is likely due to the difficulties of collecting appropriate natural samples during the dynamic phase of migration and colonization. We systematically collected blacklegged ticks (Ixodes scapularis) across New York State (NY), USA, between 2006 and 2019, a time period coinciding with a rapid range expansion of ticks and their associated pathogens including Borrelia burgdorferi, the etiological agent of Lyme disease. These samples provide a unique opportunity to investigate the population dynamics of human pathogens as they expand into novel territory. We observed that founder effects were short-lived, as gene flow from long-established populations brought almost all B. burgdorferi lineages to newly colonized populations within just a few years of colonization. By 7 years post-colonization, B. burgdorferi lineage frequency distributions were indistinguishable from long-established sites, indicating that local B. burgdorferi populations experience similar selective pressures despite geographic separation. The B. burgdorferi lineage dynamics elucidate the processes underlying the range expansion and demonstrate that migration into, and selection within, newly colonized sites operate on different time scales.

Comparative reservoir competence of Peromyscus leucopus, C57BL/6J, and C3H/HeN for Borrelia burgdorferi B31.

Borrelia burgdorferi, a Lyme disease spirochete, causes a range of acute and chronic maladies in humans. However, a primary vertebrate reservoir in the United States, the white-footed deermouse Peromyscus leucopus, is reported not to have reduced fitness following infection. Although laboratory strains of Mus musculus mice have successfully been leveraged to model acute human Lyme disease, the ability of these rodents to model B. burgdorferi-P. leucopus interactions remains understudied. Here, we compared infection of P. leucopus with B. burgdorferi B31 with infection of the traditional B. burgdorferi murine models-C57BL/6J and C3H/HeN Mus musculus, which develop signs of inflammation akin to human disease. We find that B. burgdorferi was able to reach much higher burdens (10- to 30-times higher) in multiple M. musculus skin sites and that the overall dynamics of infection differed between the two rodent species. We also found that P. leucopus remained transmissive to larval Ixodes scapularis for a far shorter period than either M. musculus strain. In line with these observations, we found that P. leucopus does launch a modest but sustained inflammatory response against B. burgdorferi in the skin, which we hypothesize leads to reduced bacterial viability and rodent-to-tick transmission in these hosts. Similarly, we also observe evidence of inflammation in infected P. leucopus hearts. These observations provide new insight into reservoir species and the B. burgdorferi enzootic cycle.IMPORTANCEA Lyme disease-causing bacteria, Borrelia burgdorferi, must alternate between infecting a vertebrate host-usually rodents or birds-and ticks. In order to be successful in that endeavor, the bacteria must avoid being killed by the vertebrate host before it can infect a new larval tick. In this work, we examine how B. burgdorferi and one of its primary vertebrate reservoirs, Peromyscus leucopus, interact during an experimental infection. We find that B. burgdorferi appears to colonize its natural host less successfully than conventional laboratory mouse models, which aligns with a sustained seemingly anti-bacterial response by P. leucopus against the microbe. These data enhance our understanding of P. leucopus host-pathogen interactions and could potentially serve as a foundation to uncover ways to disrupt the spread of B. burgdorferi in nature.

Ixodes scapularis density and Borrelia burgdorferi prevalence along a residential-woodland gradient in a region of emerging Lyme disease risk.

The environmental risk of Lyme disease, defined by the density of Ixodes scapularis ticks and their prevalence of Borrelia burgdorferi infection, is increasing across the Ottawa, Ontario region, making this a unique location to explore the factors associated with environmental risk along a residential-woodland gradient. In this study, we collected I. scapularis ticks and trapped Peromyscus spp. mice, tested both for tick-borne pathogens, and monitored the intensity of foraging activity by deer in residential, woodland, and residential-woodland interface zones of four neighbourhoods. We constructed mixed-effect models to test for site-specific characteristics associated with densities of questing nymphal and adult ticks and the infection prevalence of nymphal and adult ticks. Compared to residential zones, we found a strong increasing gradient in tick density from interface to woodland zones, with 4 and 15 times as many nymphal ticks, respectively. Infection prevalence of nymphs and adults together was 15 to 24 times greater in non-residential zone habitats. Ecological site characteristics, including soil moisture, leaf litter depth, and understory density, were associated with variations in nymphal density and their infection prevalence. Our results suggest that high environmental risk bordering residential areas poses a concern for human-tick encounters, highlighting the need for targeted disease prevention.

Lizards and the enzootic cycle of Borrelia burgdorferi sensu lato.

Emerging and re-emerging pathogens often stem from zoonotic origins, cycling between humans and animals, and are frequently vectored and maintained by hematophagous arthropod vectors. The efficiency by which these disease agents are successfully transmitted between vertebrate hosts is influenced by many factors, including the host on which a vector feeds. The Lyme disease bacterium Borrelia burgdorferi sensu lato has adapted to survive in complex host environments, vectored by Ixodes ticks, and maintained in multiple vertebrate hosts. The versatility of Lyme borreliae in disparate host milieus is a compelling platform to investigate mechanisms dictating pathogen transmission through complex networks of vertebrates and ticks. Squamata, one of the most diverse clade of extant reptiles, is comprised primarily of lizards, many of which are readily fed upon by Ixodes ticks. Yet, lizards are one of the least studied taxa at risk of contributing to the transmission and life cycle maintenance of Lyme borreliae. In this review, we summarize the current evidence, spanning from field surveillance to laboratory infection studies, supporting their contributions to Lyme borreliae circulation. We also summarize the current understanding of divergent lizard immune responses that may explain the underlying molecular mechanisms to confer Lyme spirochete survival in vertebrate hosts. This review offers a critical perspective on potential enzootic cycles existing between lizard-tick-Borrelia interactions and highlights the importance of an eco-immunology lens for zoonotic pathogen transmission studies.

A rodent and tick bait for controlling white-footed mice (Peromyscus leucopus) and blacklegged ticks (Ixodes scapularis), the respective pathogen host and vector of the Lyme disease spirochetes.

A promising alternative approach to conventional vector and rodent control practices is the use of a bait containing a rodenticide and acaricide in controlling vectors and pathogen reservoirs concurrently. In the United States, Lyme disease continues to be the most prevalent vector-borne disease with approximately 500,000 Lyme disease cases estimated each year. Previous research has demonstrated the usefulness of a low dose fipronil bait in controlling Ixodes scapularis larvae feeding on white-footed mice. However, considering white-footed mice can be an unwanted species because of their association with tick-borne disease and hantaviruses, a combination rodent and tick bait (RTB) might provide a useful alternative to encourage additional community participation in integrated tick management (ITM) efforts. The purpose of this research was to evaluate the use of RTB (0.025 % warfarin, 0.005 % fipronil) in controlling white-footed mice and I. scapularis larvae. Studies were designed in part based on Environmental Protection Agency (EPA) guidelines. A laboratory choice test was conducted to evaluate the use of RTB in controlling white-footed mice over 15-day exposure when they were exposed to an alternative diet. Mice were observed every day for mortality and signs of warfarin toxicity. A simulated field test was conducted to evaluate the use of RTB, presented in the presence of an alternative diet, in controlling I. scapularis parasitizing white-footed mice over 4-day exposure. Mice were fitted with capsules and manually infested with I. scapularis larvae. The inside of each capsule was observed to evaluate tick attachment. Replete larvae detaching from each mouse were collected. Blood was collected from all treatment group mice via cardiac puncture to determine the fipronil sulfone concentration in plasma for each animal. Results indicated that RTB would be adequately consumed in the presence of an alternative diet under laboratory and simulated field conditions. Treatment with RTB resulted in 100 % mortality of white-footed mice during 15-day exposure and prevented 100 % larvae from feeding to repletion during 4-day exposure. All mice succumbing to RTB showed signs of warfarin toxicity. All mice parasitized with ticks that were exposed to RTB had fipronil sulfone detectable in plasma, with even the lowest concentration detected (8.1 parts per billion) controlling 100 % parasitizing I. scapularis larvae. The results suggest that RTB could be a useful means of rodent and tick control for use in ITM programs.

Borrelia burgdorferi sensu lato prevalence in Ixodes scapularis from Canada: A thirty-year summary and meta-analysis (1990-2020).

Borrelia burgdorferi sensu lato (Bb) are a complex of bacteria genospecies that can cause Lyme disease (LD) in humans after the bite of an infected Ixodes spp. vector tick. In Canada, incidence of LD is increasing in part due to the rapid geographic expansion of Ixodes scapularis across the southcentral and eastern provinces. To better understand temporal and spatial (provincial) prevalence of Bb infection of I. scapularis and how tick surveillance is utilized in Canada to assess LD risk, a literature review was conducted. Tick surveillance studies published between January 1975 to November 2023, that measured the prevalence of Bb in I. scapularis via "passive surveillance" from the public citizenry or "active surveillance" by drag or flag sampling of host-seeking ticks in Canada were included for review. Meta-analyses were conducted via random effects modeling. Forty-seven articles, yielding 26 passive and 28 active surveillance studies, met inclusion criteria. Mean durations of collection for I. scapularis were 2.1 years in active surveillance studies (1999-2020) and 5.5 years by passive surveillance studies (1990-2020). Collectively, data were extracted on 99,528 I. scapularis nymphs and adults collected between 1990-2020 across nine provinces, including Newfoundland & Labrador (33 ticks) and Alberta (208 ticks). More studies were conducted in Ontario (36) than any other province. Across nine provinces, the prevalence of Bb infection in I. scapularis collected by passive surveillance was 14.6% with the highest prevalence in Nova Scotia at 20.5% (minimum studies >1). Among host-seeking I. scapularis collected via active surveillance, Bb infection prevalence was 10.5% in nymphs, 31.9% in adults, and 23.8% across both life stages. Host-seeking I. scapularis nymphs and adults from Ontario had the highest Bb prevalence at 13.6% and 34.8%, respectively. Between 2007-2019, Bb infection prevalence in host-seeking I. scapularis was positively associated over time (p<0.001) which is concurrent with a ∼25-fold increase in the number of annually reported LD cases in Canada over the same period. The prevalence of Bb-infection in I. scapularis has rapidly increased over three decades as reported by tick surveillance studies in Canada which coincides with increasing human incidence for LD. The wide-ranging distribution and variable prevalence of Bb-infected I. scapularis ticks across provinces demonstrates the growing need for long-term standardized tick surveillance to monitor the changing trends in I. scapularis populations and best define LD risk areas in Canada.

Multiple factors affecting Ixodes ricinus ticks and associated pathogens in European temperate ecosystems (northeastern France).

In Europe, the main vector of tick-borne zoonoses is Ixodes ricinus, which has three life stages. During their development cycle, ticks take three separate blood meals from a wide variety of vertebrate hosts, during which they can acquire and transmit human pathogens such as Borrelia burgdorferi sensu lato, the causative agent of Lyme borreliosis. In this study conducted in Northeastern France, we studied the importance of soil type, land use, forest stand type, and temporal dynamics on the abundance of ticks and their associated pathogens. Negative binomial regression modeling of the results indicated that limestone-based soils were more favorable to ticks than sandstone-based soils. The highest tick abundance was observed in forests, particularly among coniferous and mixed stands. We identified an effect of habitat time dynamics in forests and in wetlands: recent forests and current wetlands supported more ticks than stable forests and former wetlands, respectively. We observed a close association between tick abundance and the abundance of Cervidae, Leporidae, and birds. The tick-borne pathogens responsible for Lyme borreliosis, anaplasmosis, and hard tick relapsing fever showed specific habitat preferences and associations with specific animal families. Machine learning algorithms identified soil related variables as the best predictors of tick and pathogen abundance.

Warming, but not infection with Borrelia burgdorferi, increases off-host winter activity in the ectoparasite, Ixodes scapularis.

Warming winters will change patterns of behaviour in temperate and polar arthropods, but we know little about the drivers of winter activity in animals such as ticks. Any changes in behaviour are likely to arise from a combination of both abiotic (e.g. temperature) and biotic (e.g. infection) drivers, and will have important consequences for survival and species interactions. Blacklegged ticks, Ixodes scapularis, have invaded Atlantic Canada and high proportions (30-50%) are infected with the bacteria causing Lyme disease, Borrelia burgdorferi. Infection is correlated with increased overwintering survival of adult females, and ticks are increasingly active in the winter, but it is unclear if infection is associated with activity. Further, we know little about how temperature drives the frequency of winter activity. Here, we exposed wild-caught, adult, female Ixodes scapularis ticks to three different winter temperature regimes (constant low temperatures, increased warming, and increased warming + variability) to determine the thermal and infection conditions that promote or suppress activity. We used automated behaviour monitors to track daily activity in individual ticks and repeated the study with fresh ticks over three years. Following exposure to winter conditions we determined whether ticks were infected with the bacteria B. burgdorferi and if infection was responsible for any patterns in winter activity. Warming conditions promoted increased activity throughout the overwintering period but infection with B. burgdorferi had no impact on the frequency or overall number of ticks active throughout the winter. Individual ticks varied in their levels of activity throughout the winter, such that some were largely dormant for several weeks, while others were active almost daily; however, we do not yet know the drivers behind this individual variation in behaviour. Overall, warming winters will heighten the risk of tick-host encounters.

Out of Asia? Expansion of Eurasian Lyme borreliosis causing genospecies display unique evolutionary trajectories.

Vector-borne pathogens exist in obligate transmission cycles between vector and reservoir host species. Host and vector shifts can lead to geographic expansion of infectious agents and the emergence of new diseases in susceptible individuals. Three bacterial genospecies (Borrelia afzelii, Borrelia bavariensis, and Borrelia garinii) predominantly utilize two distinct tick species as vectors in Asia (Ixodes persulcatus) and Europe (Ixodes ricinus). Through these vectors, the bacteria can infect various vertebrate groups (e.g., rodents, birds) including humans where they cause Lyme borreliosis, the most common vector-borne disease in the Northern hemisphere. Yet, how and in which order the three Borrelia genospecies colonized each continent remains unclear including the evolutionary consequences of this geographic expansion. Here, by reconstructing the evolutionary history of 142 Eurasian isolates, we found evidence that the ancestors of each of the three genospecies probably have an Asian origin. Even so, each genospecies studied displayed a unique substructuring and evolutionary response to the colonization of Europe. The pattern of allele sharing between continents is consistent with the dispersal rate of the respective vertebrate hosts, supporting the concept that adaptation of Borrelia genospecies to the host is important for pathogen dispersal. Our results highlight that Eurasian Lyme borreliosis agents are all capable of geographic expansion with host association influencing their dispersal; further displaying the importance of host and vector association to the geographic expansion of vector-borne pathogens and potentially conditioning their capacity as emergent pathogens.

Range Expansion of Ixodes scapularis and Borrelia burgdorferi in Ontario, Canada, from 2017 to 2019.

Range expansion of the vector tick species, Ixodes scapularis, has been detected in Ontario over the last two decades. This has led to elevated risk of exposure to Borrelia burgdorferi, the bacterium that causes Lyme disease. Previous research using passive surveillance data suggests that I. scapularis populations establish before the establishment of B. burgdorferi transmission cycles, with a delay of ∼5 years. The objectives of this research were to examine spatial and temporal patterns of I. scapularis and its pathogens from 2017 to 2019 in southwestern, eastern, and central Ontario, and to explore patterns of B. burgdorferi invasion. Over the 3-year study period, drag sampling was conducted at 48 sites across Ontario. I. scapularis ticks were tested for B. burgdorferi, Borrelia miyamotoi, Anaplasma phagocytophilum, and Babesia species, including Babesia microti and Babesia odocoilei, and Powassan virus. I. scapularis was detected at 30 sites overall, 22 of which had no history of previous tick detection. B. burgdorferi was detected at nine sites, eight of which tested positive for the first time during this study and five of which had B. burgdorferi detected concurrently with initial tick detection. Tick and pathogen hotspots were identified in eastern Ontario in 2017 and 2018, respectively. These findings provide additional evidence on the range expansion and population establishment of I. scapularis in Ontario and help generate hypotheses on the invasion of B. burgdorferi in Ontario. Ongoing public health surveillance is critical to monitor changes in I. scapularis and its pathogens in Ontario.