Scapularis-borne Pathogens Research Articles

Impact of Land Use Changes and Habitat Fragmentation on the Eco-epidemiology of Tick-Borne Diseases

The incidence of tick-borne diseases has increased in recent decades and accounts for the majority of vector-borne disease cases in temperate areas of Europe, North America, and Asia. This emergence has been attributed to multiple and interactive drivers including changes in climate, land use, abundance of key hosts, and people's behaviors affecting the probability of human exposure to infected ticks. In this forum paper, we focus on how land use changes have shaped the eco-epidemiology of Ixodes scapularis-borne pathogens, in particular the Lyme disease spirochete Borrelia burgdorferi sensu stricto in the eastern United States. We use this as a model system, addressing other tick-borne disease systems as needed to illustrate patterns or processes. We first examine how land use interacts with abiotic conditions (microclimate) and biotic factors (e.g., host community composition) to influence the enzootic hazard, measured as the density of host-seeking I. scapularis nymphs infected with B. burgdorferi s.s. We then review the evidence of how specific landscape configuration, in particular forest fragmentation, influences the enzootic hazard and disease risk across spatial scales and urbanization levels. We emphasize the need for a dynamic understanding of landscapes based on tick and pathogen host movement and habitat use in relation to human resource provisioning. We propose a coupled natural-human systems framework for tick-borne diseases that accounts for the multiple interactions, nonlinearities and feedbacks in the system and conclude with a call for standardization of methodology and terminology to help integrate studies conducted at multiple scales.

An Acarological Risk Model Predicting the Density and Distribution of Host-Seeking Ixodes scapularis Nymphs in Minnesota.

.Ixodes scapularis is the vector of at least seven human pathogens in Minnesota, two of which are known to cause Lyme disease (Borrelia burgdorferi sensu stricto and Borrelia mayonii). In Minnesota, the statewide incidence of Lyme disease and other I. scapularis–borne diseases and the geographic extent over which cases have been reported have both increased substantially over the last two decades. These changes correspond with an expanding distribution of I. scapularis over a similar time frame. Because the risk of exposure to I. scapularis–borne pathogens is likely related to the number of ticks encountered, we developed an acarological risk model predicting the density of host-seeking I. scapularis nymphs (DON) in Minnesota. The model was informed by sampling 81 sites located in 42 counties in Minnesota. Two main foci were predicted by the model to support elevated densities of host-seeking I. scapularis nymphs, which included the seven-county Minneapolis-St. Paul metropolitan area and counties in northern Minnesota, including Lake of the Woods and Koochiching counties. There was substantial heterogeneity observed in predicted DON across the state at the county scale; however, counties classified as high risk for I. scapularis–borne diseases and counties with known established populations of I. scapularis had the highest proportion of the county predicted as suitable for host-seeking nymphs (≥ 0.13 nymphs/100 m2). The model provides insight into areas of potential I. scapularis population expansion and identifies focal areas of predicted suitable habitat within counties where the incidence of I. scapularis–borne diseases has been historically low.

Northward range expansion of Ixodes scapularis evident over a short timescale in Ontario, Canada.

The invasion of the blacklegged tick, Ixodes scapularis into Ontario, Canada poses a significant risk to public health because it is a vector for numerous pathogens, including Borrelia burgdorferi sensu stricto, the causative agent of Lyme disease. Baseline field sampling in 2014 and 2015 detected I. scapularis and B. burgdorferi at sites across southern, eastern and central Ontario, including a hot spot in eastern Ontario. A “speed of spread” model for I. scapularis developed by Leighton and colleagues (2012) estimated that the tick’s range was expanding northward at 46 km/year. In 2016, we revisited a subset of sites sampled in 2014 and 2015 to understand the changing nature of risk, and assess whether the rate of tick invasion is consistent with the speed of spread estimate. Ticks were collected via tick dragging at 17 out of 36 sites, 5 of which were new sites for I. scapularis. Samples were positive for B. burgdorferi at 8 sites. No other I. scapularis-borne pathogens were detected. Centrographic statistics revealed an increase in the dispersion of I. scapularis positive sites in eastern Ontario. Field data for each site were then compared to the model’s predicted year of establishment for each census subdivision. Our findings illustrate that the range expansion of I. scapularis and the emergence of B. burgdorferi is ongoing, and provide short timescale evidence of the processes associated with I. scapularis spread. The range front appears to be moving at a rate of ~46 km/year, with colonization of the tick behind this range front occurring at a slower and heterogeneous rate. Assessment of site-level ecological factors did not provide any insight into the underlying processes that may be influencing the colonization of I. scapularis in specific areas. Ongoing field sampling is needed to monitor this dynamic process. This study highlights the current geographic risk associated with Lyme disease, which can be used to target public health interventions to the areas of greatest risk.

A historical snapshot of Ixodes scapularis-borne pathogens in New Jersey ticks reflects a changing disease landscape

Historical specimens, when available, can provide new insight into the distribution and evolution of pathogens that may not be discernible from more recent samples. We used ticks collected from hunter-killed white-tailed deer in New Jersey in 2002 to examine the prevalence and distribution of four pathogens transmitted by Ixodes scapularis, the blacklegged tick. Infection with Borrelia burgdorferi sensu stricto, Babesia microti, and Anaplasma phagocytophilum (the agents of Lyme disease, human babesiosis, and human granulocytic anaplasmosis, respectively) was highest in the Coastal Plain and lowest in the northwestern Skylands region. These patterns correspond well with the historically observed northward expansion of I. scapularis within New Jersey and the comparatively recent increase in human cases of these pathogens in the northern part of the state. Additionally, we provide evidence that Borrelia miyamotoi, a relatively new emerging pathogen and agent of relapsing fever, was widespread (though not common) throughout the state in 2002. Our findings highlight the need for enhanced awareness of tick-borne diseases other than Lyme and implementation of large-scale tick surveillance in endemic regions.

Evaluating acarological risk for exposure to Ixodes scapularis and Ixodes scapularis-borne pathogens in recreational and residential settings in Washington County, Minnesota

The distribution of I. scapularis, the tick vector of the bacteria that cause Lyme disease, has been expanding over the last two decades in the north-central United States in parallel with increasing incidence of human cases of Lyme disease in that region. However, assessments of residential risk for exposure to ticks are lacking from this region. Here, we measured the density of host-seeking I. scapularis nymphs in two suburban and two rural public recreational sites located in Washington County, Minnesota as well as in nearby residential properties. We sought to compare tick densities across land use types and to identify environmental factors that might impact nymphal density. We also assessed the prevalence of infection in the collected ticks with Lyme disease spirochetes (Borrelia burgdorferi sensu stricto, B. mayonii), and other I. scapularis-borne pathogens including B. miyamotoi, Babesia microti and Anaplasma phagocytophilum. Similar to studies from the eastern United States, on residential properties, I. scapularis nymphal densities were highest in the ecotonal areas between the forest edge and the lawn. Residences with the highest densities of nymphs were more likely to have a higher percentage of forest cover, log piles, and signs of deer on their property. In recreational areas, we found the highest nymphal densities both in the wooded areas next to trails as well as on mowed trails. Among the 303 host-seeking I. scapularis nymphs tested for pathogens, B. burgdorferi sensu stricto, A. phagocytophilum and B. miyamotoi were detected in 42 (13.8%), 14 (4.6%), and 2 (0.6%) nymphs, respectively.

Increased diversity of zoonotic pathogens and Borrelia burgdorferi strains in established versus incipient Ixodes scapularis populations across the Midwestern United States

The center of origin theory predicts that genetic diversity will be greatest near a specie’s geographic origin because of the length of time for evolution. By corollary, diversity will decrease with distance from the origin; furthermore, invasion and colonization are frequently associated with founder effects that reduce genetic variation in incipient populations. The blacklegged tick, Ixodes scapularis, harbors a suite of zoonotic pathogens, and the geographic range of the tick is expanding in the upper Midwestern United States. Therefore, we posited that diversity of I. scapularis-borne pathogens across its Midwestern range should correlate with the rate of the range expansion of this tick as well as subsequent disease emergence. Analysis of 1565 adult I. scapularis ticks from 13 sites across five Midwestern states revealed that tick infection prevalence with multiple microbial agents (Borrelia burgdorferi, Borrelia miyamotoi, Babesia odocoilei, Babesia microti, and Anaplasma phagocytophilum), coinfections, and molecular genetic diversity of B. burgdorferi all were positively correlated with the duration of establishment of tick populations, and therefore generally support the center of origin – pathogen diversity hypothesis. The observed differences across the gradient of establishment, however, were not strong and were nuanced by the high frequency of coinfections in tick populations at both established and recently-invaded tick populations. These results suggest that the invasion of ticks and their associated pathogens likely involve multiple means of pathogen introduction, rather than the conventionally presented scenario whereby infected, invading ticks are solely responsible for introducing pathogens to naïve host populations.

Investigation of the Population Structure of the Tick Vector of Lyme DiseaseIxodes scapularis(Acari: Ixodidae) in Canada Using Mitochondrial Cytochrome C Oxidase Subunit I Gene Sequences

Genotyping of Ixodes scapularis Say (Acari: Ixodidae) ticks could enhance understanding of the occurrence and genotypes of I. scapularis-borne pathogens. We investigated the utility of mitochondrial (mt) Cytochrome C Oxidase subunit I gene (cox1) sequences as a tool for understanding the population structure of I. scapularis collected in Canada, where we also investigated the geographic occurrence of different cox1 haplotypes. Sequences obtained from 414 ticks were one of 55 unique haplotypes, most of which grouped into one of six clades. Demographic analysis suggested that cox1 sequences have haplotype and nucleotide diversity comparable to other mt genes. All haplotypes were connected in a single minimum spanning network tree. Despite low fixation index values there were significant differences in the frequency of occurrence of haplotypes of different clades among four geographic regions: 1) Alberta to western Ontario, 2) eastern Ontario, 3) Quebec, and 4) Atlantic Provinces; suggesting that cox1 sequences could reveal population structure differences between I. scapularis in geographically separated populations of northeastern and midwestern North America. Spatial clusters of ticks of the same haplotype identified in regions of southern Quebec and southern Ontario where I. scapularis is invading were consistent with population bottlenecks associated with founder events. These findings suggest that cox1 sequences are useful for the study of I. scapularis population structure, are of sufficient diversity that spatial analyses of haplotypes can be used to identify where I. scapularis is emerging in southern Canada, and may be useful for exploring differences between northeastern and midwestern populations of I. scapularis.

Projected effects of climate change on tick phenology and fitness of pathogens transmitted by the North American tick Ixodes scapularis

Ixodes scapularis is the principal tick vector of the Lyme borreliosis agent Borrelia burgdorferi and other tick-borne zoonoses in northeastern North America. The degree of seasonal synchrony of nymphal and larval ticks may be important in influencing the basic reproductive number of the pathogens transmitted by I. scapularis. Because the seasonal phenology of tick vectors is partly controlled by ambient temperature, climate and climate change could shape the population biology of tick-borne pathogens. We used projected monthly normal temperatures, obtained from the second version of the Canadian Coupled Global Climate Model (CGCM2) under emissions scenario A2 of the Intergovernmental Panel on Climate Change for a site in southern Ontario, Canada, to simulate the phenology of I. scapularis in a mathematical model. The simulated seasonal abundance of ticks then determined transmission of three candidate pathogens amongst a population of white-footed mice (Peromyscus leucopus) using a susceptible–infected–recovered (SIR) model. Fitness of the different pathogens, in terms of resilience to changes in tick and rodent mortality, minima for infection duration, transmission efficiency and particularly any additional mortality of rodents specifically associated with infection, varied according to the seasonal pattern of immature tick activity, which was different under the temperature conditions projected for the 2020s, 2050s and 2080s. In each case, pathogens that were long-lived, highly transmissible and had little impact on rodent mortality rates were the fittest. However, under the seasonal tick activity patterns projected for the 2020s and 2050s, the fitness of pathogens that are shorter-lived, less efficiently transmitted, and more pathogenic to their natural hosts, increased. Therefore, climate change may affect the frequency and distribution of I. scapularis-borne pathogens and alter their evolutionary trajectories.