Invasion of Two Tick-borne Diseases Across New England: Harnessing Human Surveillance Data to Capture Underlying Ecological Invasion Processes

Modelling the spatial spread of vector-borne zoonotic pathogens maintained in enzootic transmission cycles remains a major challenge. The best available spatio-temporal data on pathogen spread often take the form of human disease surveillance data. By applying a classic ecological approach-occupancy modelling-to an epidemiological question of disease spread, we used surveillance data to examine the latent ecological invasion of tick-borne pathogens. Over the last half-century, previously undescribed tick-borne pathogens including the agents of Lyme disease and human babesiosis have rapidly spread across the northeast United States. Despite their epidemiological importance, the mechanisms of tick-borne pathogen invasion and drivers underlying the distinct invasion trajectories of the co-vectored pathogens remain unresolved. Our approach allowed us to estimate the unobserved ecological processes underlying pathogen spread while accounting for imperfect detection of human cases. Our model predicts that tick-borne diseases spread in a diffusion-like manner with occasional long-distance dispersal and that babesiosis spread exhibits strong dependence on Lyme disease

The Interface Between Invasive Species and the Increased Incidence of Tick-borne Diseases, and the Implications for Federal Land Managers

Includes information on the dynamics of tick-borne disease, factors affecting the occurrence and density of ticks, matrices of ties between habitat, human activities, invasive plants, and ticks, federal resources and programs related to ticks and vector-borne disease in the United States, with references and an annotated bibliography of literature on ticks, vector-borne diseases, and invasive species

Changing geographic ranges of ticks and tick-borne pathogens: drivers, mechanisms and consequences for pathogen diversity

The geographic ranges of ticks and tick-borne pathogens are changing due to global and local environmental (including climatic) changes. In this review we explore current knowledge of the drivers for changes in the ranges of ticks and tick-borne pathogen species and strains via effects on their basic reproduction number (R-0), and the mechanisms of dispersal that allow ticks and tick-borne pathogens to invade suitable environments. Using the expanding geographic distribution of the vectors and agent of Lyme disease as an example we then investigate what could be expected of the diversity of tick-borne pathogens during the process of range expansion, and compare this with what is currently being observed. Lastly we explore how historic population and range expansions and contractions could be reflected in the phylogeography of ticks and tick-borne pathogens seen in recent years, and conclude that combined study of currently changing tick and tick-borne pathogen ranges and diversity, with phylogeographic analysis, may help us better predict future patterns of invasion and diversity

The effects of global climate change and habitat modification on the incidence of Lyme disease

Lyme disease is one of the most common vector-borne diseases around the world, and the numbers of reported cases are quickly rising. Ixodes ticks are the principal vectors, while Borrelia burgdorferi sensu lato genospecies are the etiological agents of the disease. Climate change, namely global warming, and habitat modification, namely forest fragmentation, are hypothesized to play an active role in this rise in reported cases. An analysis of the primary literature, specifically of studies focused on North America and Europe, was conducted in order to investigate these hypotheses. These studies show that global warming has precipitated a growth in tick populations as well as a northward tick migration, thereby increasing the risk of Lyme disease in emergent and endemic areas alike, for Borrelia spirochetes quickly infect naïve tick populations. Furthermore, published studies support the idea that forest fragmentation near human population centers has also increased the risk of Lyme disease in North America, for edge habitats provide suitable conditions for ticks and provide edible vegetation for the animals on which ticks feed, animals which also serve as hosts for B. burgdorferi sensu lato. In contrast, a decrease in fragmentation was found to facilitate tick invasion and establishment in Europe. These studies demonstrate that anthropogenic habitat modifications of varying types can affect ticks and their host populations and increase the risk of Lyme disease near human population centers. However, more research needs to be done to truly understand the different factors that are precipitating the rising number of cases of Lyme disease since there are significant interactions between climate change, habitat modification, and other drivers not examined here. Furthermore, understanding how these drivers function in specific geographic locations can help scientists and public officials tailor local public health measures appropriately. Finally, researchers and pharmaceutical companies must develop a safe, long-lasting, and effective vaccine against the Lyme disease spirochete, for there is not one currently available. Although easily treatable if diagnosed early, Lyme disease can progress to debilitating disease. Unfortunately, the risk of contracting this illness is currently rising and will continue to rise unless effective preventative measures are employed

Assembling evidence for identifying reservoirs of infection

Many pathogens persist in multihost systems, making the identification of infection reservoirs crucial for devising effective interventions. Here, we present a conceptual framework for classifying patterns of incidence and prevalence, and review recent scientific advances that allow us to study and manage reservoirs simultaneously. We argue that interventions can have a crucial role in enriching our mechanistic understanding of how reservoirs function and should be embedded as quasi-experimental studies in adaptive management frameworks. Single approaches to the study of reservoirs are unlikely to generate conclusive insights whereas the formal integration of data and methodologies, involving interventions, pathogen genetics, and contemporary surveillance techniques, promises to open up new opportunities to advance understanding of complex multihost systems

Blacklegged Tick (\u3cem\u3eIxodes scapularis\u3c/em\u3e) Distribution in Maine, USA, as Related to Climate Change, White-tailed Deer, and the Landscape

Lyme disease is caused by the bacterial spirochete Borrelia burgdorferi, which is transmitted through the bite of an infected blacklegged (deer) tick (Ixodes scapularis). Geographic invasion of I. scapularis in North America has been attributed to causes including 20th century reforestation and suburbanization, burgeoning populations of the white-tailed deer (Odocoileus virginianus) which is the primary reproductive host of I. scapularis, tick-associated non-native plant invasions, and climate change. Maine, USA, is a high Lyme disease incidence state, with a history of increasing I. scapularis abundance and northward range expansion. This thesis addresses the question: “To what extent has the range expansion of blacklegged ticks in Maine been associated with climate change, deer, and other factors?” using a long-term, passive surveillance dataset (1990-2013) of I. scapularis in Maine. Chapter 1 characterized temporal trends in I. scapularis submissions rate (an index of abundance) and phenology, in Maine’s northern (7 counties) versus southern (9 counties) tier. In the northern tier the I. scapularis submission rate and season duration increased throughout the duration of the time series, indicating I. scapularis was emergent but not established. By contrast, in the southern tier, submissions rate and season duration increased initially but after about 13 years leveled off, indicating I. scapularis was established by the mid-2000s. Winter and fall average minimum temperatures increased in the northern tier and summer relative humidity in both tiers increased. I. scapularis submission rates and phenological changes were correlated with relative humidity statewide. Generally, I. scapularis submission rates and phenological changes were correlated with winter warming, but predominantly in the northern tier and only the early half of the time series for the southern tier. Though northern tier climate appears to have become more permissive over time, current ecological suitability for I. scapularis in the northern tier may be limited due to low deer densities, which averaged ~5/mi2. In the southern tier, deer densities were higher and correlated with I. scapularis submissions rate. However, a number of other, unknown population-limiting mechanisms could have been operating to keep I. scapularis in the southern tier at a dynamic equilibrium since the mid-2000s. Also observed was a correlation between Lyme incidence and I. scapularis in the northern but not southern tier. This may represent decoupling of reported disease incidence and entomological risk as measured simply by tick abundance and Borrelial infection prevalence. This discrepancy suggested that disease discovery had increased through greater clinician and patient awareness and testing effort, and/or that acarological risk may be a more nuanced function of diverse, variously virulent strain types in multiple pathogens borne by I. scapularis. Chapter 2 used a generalized additive mixed model (GAMM) to model linear and nonlinear relationships between nymphal I. scapularis abundance and predictors, while allowing for spatiotemporal dependencies within and among wildlife management districts. I. scapularis nymphs increased with increasing deer densities up to ~13 deer/mi2, but beyond this threshold tick abundance did not vary with deer density. This result corroborated the idea of a saturating relationship between I. scapularis and deer density. It was also consistent with empirical studies suggesting deer density must be lowered below ~8-13/mi2 to lower I. scapularis abundance enough to lower Lyme disease. The model also indicated that more ticks were associated with higher relative humidity, warmer minimum winter temperatures and more degree-day accumulation, and that without deer \u3e4/mi2 warmer winters would not increase nymphal abundance. The Maine Department of Inland Fisheries and Wildlife northern tier goals range from 10-15/mi2 and southern tier goals from 15-20/mi2 for 2030 (MEIFW 2017). We recommended deer densities be kept to ≤10/mi2 in all of Maine’s northern tier to mitigate likely increases in ticks due to future warming. Suburbanization and presence of tick-associated non-native plants did not enter the model because they co-occurred with deer. Chapter 3 ascertained that Lyme incidences on the off-shore, unbridged islands of Maine have been above the statewide average and at least on par with those seen on other offshore islands in Massachusetts and Rhode Island. Increasing I. scapularis abundance and Lyme incidence have been attributed to high deer densities by some residents of these island communities. Burgeoning deer densities on some of these islands have led to various deer management histories along with a good deal of conflict on how to manage deer populations. We summarized the burden of Lyme disease, entomological risk, and deer management histories on these islands. We also polled island residents in 2016 to quantify the level of concern about the Lyme disease problem and assess the level of support for deer herd reduction on their islands. A 2016 survey of island residents indicated that other deer-related problems, namely vehicle collisions and garden and forest damage, motivated support for deer reduction as much as Lyme disease. We recommended efforts to keep deer density ≤15/mi2 and to remove invasive plant species--particular Japanese barberry—from the landscape. The benefits of these measures will extend beyond vector tick control to improved deer and forest health

Predictors Of Babesia Microti Infection In Ixodes Scapularis Ticks In New England, Usa

Babesia microti is the primary etiological agent of human babesiosis (Vannier & Krause). Although it shares the same tick vector and mammal reservoirs as B. burgdorferi, the causative agent of Lyme disease, the geographic extent of B. microti is limited to a subset of the range of B. burgdorferi (Diuk-Wasser et al.). Despite the slower spread of B. microti, it is equally prevalent in ticks in certain areas where both B. burgdorferi and B. microti have been endemic for long periods. The slower rate of B. microti expansion as compared to B. burgdorferi has been attributed to a lower efficiency of transmission for B. microti (Dunn et al.), however, this alone does not explain the similar prevalence of both microbes in areas long endemic to both pathogens. This study assesses the relative importance of ecological conditions and pathogen interactions in B. microti and B. burgdorferi prevalence in I. scapularis nymphs from a sample of 1514 nymph-stage ticks collected at 35 sites in eastern Connecticut, western Rhode Island, and southern Massachusetts. Our results show that the odds of a tick testing positive for B. microti is not associated to the density of nymphal ticks or the prevalence of B. burgdorferi at the site level, but it is associated with the presence of B. burgdorferi in the individual tick and the geographic location of the tick. None of the covariates tested showed a strong association with the odds of a tick testing positive for B. burgdorferi

Past and future perspectives on mathematical models of tick-borne pathogens

Ticks are vectors of pathogens which are important both with respect to human health and economically. They have a complex lifecycle requiring several blood meals throughout their life. These blood meals take place on different individual hosts and potentially on different host species. Their lifecycle is also dependent on environmental conditions such as the temperature and habitat type. Mathematical models have been used for the more than 30 years to help us understand how tick dynamics are dependent on these environmental factors and host availability. In this paper we review models of tick dynamics and summarise the main results. This summary is split into two parts, one which looks at tick dynamics and one which looks at tick borne-pathogens. In general, the models of tick dynamics are used to determine when the peak in tick densities is likely to occur in the year and how that changes with environmental conditions. The models of tick borne pathogens focus more on the conditions under which the pathogen can persist and how host population densities might be manipulated to control these pathogens. In the final section of the paper we identify gaps in the current knowledge and future modelling approaches