Patrick A. Leighton

Estimated Effects of Projected Climate Change on the Basic Reproductive Number of the Lyme Disease Vector Ixodes scapularis

Background: The extent to which climate change may affect human health by increasing risk from vector-borne diseases has been under considerable debate. Objectives: We quantified potential effects of future climate change on the basic reproduction number (R0) of the tick vector of Lyme disease, Ixodes scapularis, and explored their importance for Lyme disease risk, and for vector-borne diseases in general. Methods: We applied observed temperature data for North America and projected temperatures using regional climate models to drive an I. scapularis population model to hindcast recent, and project future, effects of climate warming on R0. Modeled R0 increases were compared with R0 ranges for pathogens and parasites associated with variations in key ecological and epidemiological factors (obtained by literature review) to assess their epidemiological importance. Results: R0 for I. scapularis in North America increased during the years 1971–2010 in spatio-temporal patterns consistent with observations. Increased temperatures due to projected climate change increased R0 by factors (2–5 times in Canada and 1.5–2 times in the United States), comparable to observed ranges of R0 for pathogens and parasites due to variations in strains, geographic locations, epidemics, host and vector densities, and control efforts. Conclusions: Climate warming may have co-driven the emergence of Lyme disease in northeastern North America, and in the future may drive substantial disease spread into new geographic regions and increase tick-borne disease risk where climate is currently suitable. Our findings highlight the potential for climate change to have profound effects on vectors and vector-borne diseases, and the need to refocus efforts to understand these effects. Citation: Ogden NH, Radojević M, Wu X, Duvvuri VR, Leighton PA, Wu J. 2014. Estimated effects of projected climate change on the basic reproductive number of the Lyme disease vector Ixodes scapularis. Environ Health Perspect 122:631–638; http://dx.doi.org/10.1289/ehp.1307799

Climate change and habitat fragmentation drive the occurrence of Borrelia burgdorferi, the agent of Lyme disease, at the northeastern limit of its distribution

Lyme borreliosis is rapidly emerging in Canada, and climate change is likely a key driver of the northern spread of the disease in North America. We used field and modeling approaches to predict the risk of occurrence of Borrelia burgdorferi, the bacteria causing Lyme disease in North America. We combined climatic and landscape variables to model the current and future (2050) potential distribution of the black‐legged tick and the white‐footed mouse at the northeastern range limit of Lyme disease and estimated a risk index for B. burgdorferi from these distributions. The risk index was mostly constrained by the distribution of the white‐footed mouse, driven by winter climatic conditions. The next factor contributing to the risk index was the distribution of the black‐legged tick, estimated from the temperature. Landscape variables such as forest habitat and connectivity contributed little to the risk index. We predict a further northern expansion of B. burgdorferi of approximately 250–500 km by 2050 – a rate of 3.5–11 km per year – and identify areas of rapid rise in the risk of occurrence of B. burgdorferi. Our results will improve understanding of the spread of Lyme disease and inform management strategies at the most northern limit of its distribution.

Passive surveillance for I. scapularis ticks: enhanced analysis for early detection of emerging Lyme disease risk.

ABSTRACT Lyme disease (LD) is emerging in Canada because of the northward expansion of the geographic range of the tick vector Ixodes scapularis (Say). Early detection of emerging areas of LD risk is critical to public health responses, but the methods to do so on a local scale are lacking. Passive tick surveillance has operated in Canada since 1990 but this method lacks specificity for identifying areas where tick populations are established because of dispersion of ticks from established LD risk areas by migratory birds. Using data from 70 field sites in Quebec visited previously, we developed a logistic regression model for estimating the risk of I. scapularis population establishment based on the number of ticks submitted in passive surveillance and a model-derived environmental suitability index. Sensitivity-specificity plots were used to select an optimal threshold value of the linear predictor from the model as the signal for tick population establishment. This value was used to produce an “Alert Map” identifying areas where the passive surveillance data suggested ticks were establishing in Quebec. Alert Map predictions were validated by field surveillance at 76 sites: the prevalence of established I. scapularis populations was significantly greater in areas predicted as high-risk by the Alert map (29 out of 48) than in areas predicted as moderate-risk (4 out of 30) (P < 0.001). This study suggests that Alert Maps created using this approach can provide a usefully rapid and accurate tool for early identification of emerging areas of LD risk at a geographic scale appropriate for local disease control and prevention activities.

Geography, Deer, and Host Biodiversity Shape the Pattern of Lyme Disease Emergence in the Thousand Islands Archipelago of Ontario, Canada

In the Thousand Islands region of eastern Ontario, Canada, Lyme disease is emerging as a serious health risk. The factors that influence Lyme disease risk, as measured by the number of blacklegged tick (Ixodes scapularis) vectors infected with Borrelia burgdorferi, are complex and vary across eastern North America. Despite study sites in the Thousand Islands being in close geographic proximity, host communities differed and both the abundance of ticks and the prevalence of B. burgdorferi infection in them varied among sites. Using this archipelago in a natural experiment, we examined the relative importance of various biotic and abiotic factors, including air temperature, vegetation, and host communities on Lyme disease risk in this zone of recent invasion. Deer abundance and temperature at ground level were positively associated with tick abundance, whereas the number of ticks in the environment, the prevalence of B. burgdorferi infection, and the number of infected nymphs all decreased with increasing distance from the United States, the presumed source of this new endemic population of ticks. Higher species richness was associated with a lower number of infected nymphs. However, the relative abundance of Peromyscus leucopus was an important factor in modulating the effects of species richness such that high biodiversity did not always reduce the number of nymphs or the prevalence of B. burgdorferi infection. Our study is one of the first to consider the interaction between the relative abundance of small mammal hosts and species richness in the analysis of the effects of biodiversity on disease risk, providing validation for theoretical models showing both dilution and amplification effects. Insights into the B. burgdorferi transmission cycle in this zone of recent invasion will also help in devising management strategies as this important vector-borne disease expands its range in North America.

Does high biodiversity reduce the risk of Lyme disease invasion

BackgroundIt has been suggested that increasing biodiversity, specifically host diversity, reduces pathogen and parasite transmission amongst wildlife (causing a “dilution effect”), whereby transmission amongst efficient reservoir hosts, (e.g. Peromyscus spp. mice for the agent of Lyme disease Borrelia burgdorferi) is reduced by the presence of other less efficient host species. If so, then increasing biodiversity should inhibit pathogen and parasite invasion.MethodsWe investigated this hypothesis by studying invasion of B. burgdorferi and its tick vector Ixodes scapularis in 71 field sites in southeastern Canada. Indices of trapped rodent host diversity, and of biodiversity of the wider community, were investigated as variables explaining the numbers of I. scapularis collected and B. burgdorferi infection in these ticks. A wide range of alternative environmental explanatory variables were also considered.ResultsThe observation of low I. scapularis abundance and low B. burgdorferi infection prevalence in sites where I. scapularis were detected was consistent with early-stage invasion of the vector. There were significant associations between the abundance of ticks and season, year of study and ambient temperature. Abundance of host-seeking larvae was significantly associated with deer density, and abundance of host-seeking larvae and nymphs were positively associated with litter layer depth. Larval host infestations were lower where the relative proportion of non-Peromyscus spp. was high. Infestations of hosts with nymphs were lower when host species richness was higher, but overall nymphal abundance increased with species richness because Peromyscus spp. mouse abundance and host species richness were positively correlated. Nymphal infestations of hosts were lower where tree species richness was higher. B. burgdorferi infection prevalence in ticks varied significantly with an index of rates of migratory bird-borne vector and pathogen invasion.ConclusionsI. scapularis abundance and B. burgdorferi prevalence varied with explanatory variables in patterns consistent with the known biology of these species in general, and in the study region in particular. The evidence for a negative effect of host biodiversity on I. scapularis invasion was mixed. However, some evidence suggests that community biodiversity beyond just host diversity may have direct or indirect inhibitory effects on parasite invasion that warrant further study.

Harvested White-Tailed Deer as Sentinel Hosts for Early Establishing Ixodes scapularis Populations and Risk from Vector-Borne Zoonoses in Southeastern Canada

ABSTRACT Due to recent establishment of the blacklegged tick, Ixodes scapularis Say, in southeastern Canada, tick-borne zoonoses (Lyme disease, human granulocytotropic anaplasmosis, and babesiosis) are of growing concern forpublic health. Using white-tailed deer (Odocoileus virginianus) culled in southwestern Quebec during 2007–2008, we investigated whether hunter-killed deer could act as sentinels for early establishing tick populations and for tick-borne pathogens. Accounting for environmental characteristics of culling sites, and age and sex of deer, we investigated whether their tick infestation levels could identify locations of known tick populations detected in active surveillance, presumed tick populations detected by passive surveillance, or both. We also used spatial cluster analyses to identify spatial patterns of tick infestation and occurrence of tick-borne zoonoses infection in ticks collected from the deer. Adult ticks were found on 15% of the 583 deer examined. Adult male deer had the greatest number (≈90%) of adult ticks. Overall, 3, 15, and 0% of the ticks collected were polymerase chain reaction (PCR)-positive for Borrelia burgdorferi, Anaplasma phagocytophilum, and Babesia microti, respectively. Our statistical analyses suggest that sex and age of deer, temperature, precipitation, and an index of tick dispersion by migratory birds were significantly associated with tick infestation levels. Cluster analysis identified significant clusters of deer carrying ticks PCR-positive for A. phagocytophilum, and for deer carrying two or more I. scapularis. Our study suggests that hunterkilled deer may be effective as sentinels for emerging areas of tick-borne anaplasmosis. They may have limited use as sentinels for early emerging I. scapularis tick populations and emerging Lyme disease risk.

Evolutionary Aspects of Emerging Lyme Disease in Canada

ABSTRACT In North America, Lyme disease (LD) is a tick-borne zoonosis caused by the spirochete bacterium Borrelia burgdorferi sensu stricto, which is maintained by wildlife. Tick vectors and bacteria are currently spreading into Canada and causing increasing numbers of cases of LD in humans and raising a pressing need for public health responses. There is no vaccine, and LD prevention depends on knowing who is at risk and informing them how to protect themselves from infection. Recently, it was found in the United States that some strains of B. burgdorferi sensu stricto cause severe disease, whereas others cause mild, self-limiting disease. While many strains occurring in the United States also occur in Canada, strains in some parts of Canada are different from those in the United States. We therefore recognize a need to identify which strains specific to Canada can cause severe disease and to characterize their geographic distribution to determine which Canadians are particularly at risk. In this review, we summarize the history of emergence of LD in North America, our current knowledge of B. burgdorferi sensu stricto diversity, its intriguing origins in the ecology and evolution of the bacterium, and its importance for the epidemiology and clinical and laboratory diagnosis of LD. We propose methods for investigating associations between B. burgdorferi sensu stricto diversity, ecology, and pathogenicity and for developing predictive tools to guide public health interventions. We also highlight the emergence of B. burgdorferi sensu stricto in Canada as a unique opportunity for exploring the evolutionary aspects of tick-borne pathogen emergence.

Analysis of the human population bitten by Ixodes scapularis ticks in Quebec, Canada: Increasing risk of Lyme disease

Ixodes scapularis, the main vector of Borrelia burgdorferi, the spirochetal agent of Lyme disease, is expanding its range in southern Canada and bringing risk to the public from Lyme disease. The aims of this study were to (i) describe how risk of Lyme disease in Quebec, Canada, has changed from 2008 to 2014 by analysis of the number of tick submissions, the geographic scope of ticks submitted and the prevalence of B. burgdorferi in ticks removed from people and submitted through the Quebec passive tick surveillance program and (ii) explore whether exposure to ticks is influenced by age and sex. Ticks were collected from 2008 to 2014 in a passive surveillance program conducted by the Laboratoire de santé publique du Québec (LSPQ), and tested by PCR for B. burgdorferi at the National Microbiology Laboratory. The number of ticks submitted each year more than quadrupled during the study period (from 174 in 2008 to 962 in 2014), increases in the geographic range and geographic uniformity of submissions amongst municipalities were observed, and infection prevalence in the ticks (mostly adult females) submitted rose from 5.9% in 2008 to 18.1% in 2014. These data are consistent with outcomes from active surveillance for blacklegged ticks. More men (54.4%) than women (45.6%) were bitten by I. scapularis ticks and the frequency of tick submission was highest in children under 15 years of age and in the adults 50-70 years old. These findings demonstrate the utility of conducting passive tick surveillance using humans and provides information on risk groups (i.e., males, children under 15, adults older than 50, and those living in the more southern parts of the province) to which information on personal protection and tick-bite prevention should be most strongly targeted.

Passive Tick Surveillance Provides an Accurate Early Signal of Emerging Lyme Disease Risk and Human Cases in Southern Canada

Abstract Lyme disease is an emerging public health threat in Canada. In this context, rapid detection of new risk areas is essential for timely application of prevention and control measures. In Canada, information on Lyme disease risk is collected through three surveillance activities: active tick surveillance, passive tick surveillance, and reported human cases. However, each method has shortcomings that limit its ability to rapidly and reliably identify new risk areas. We investigated the relationships between risk signals provided by human cases, passive and active tick surveillance to assess the performance of tick surveillance for early detection of emerging risk areas. We used regression models to investigate the relationships between the reported human cases, Ixodes scapularis (Say; Acari: Ixodidae) ticks collected on humans through passive surveillance and the density of nymphs collected by active surveillance from 2009 to 2014 in the province of Quebec. We then developed new risk indicators and validated their ability to discriminate risk levels used by provincial public health authorities. While there was a significant positive relationship between the risk signals provided all three surveillance methods, the strongest association was between passive tick surveillance and reported human cases. Passive tick submissions were a reasonable indicator of the abundance of ticks in the environment (sensitivity and specificity [Se and Sp] < 0.70), but were a much better indicator of municipalities with more than three human cases reported over 5 yr (Se = 0.88; Sp = 0.90). These results suggest that passive tick surveillance provides a timely and reliable signal of emerging risk areas for Lyme disease in Canada.

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.