François Milord

Active and Passive Surveillance and Phylogenetic Analysis of Borrelia burgdorferi Elucidate the Process of Lyme Disease Risk Emergence in Canada

Background Northward expansion of the tick Ixodes scapularis is driving Lyme disease (LD) emergence in Canada. Information on mechanisms involved is needed to enhance surveillance and identify where LD risk is emerging. Objectives We used passive and active surveillance and phylogeographic analysis of Borrelia burgdorferi to investigate LD risk emergence in Quebec. Methods In active surveillance, we collected ticks from the environment and from captured rodents. B. burgdorferi transmission was detected by serological analysis of rodents and by polymerase chain reaction assays of ticks. Spatiotemporal trends in passive surveillance data assisted interpretation of active surveillance. Multilocus sequence typing (MLST) of B. burgdorferi in ticks identified likely source locations of B. burgdorferi. Results In active surveillance, we found I. scapularis at 55% of sites, and we were more likely to find them at sites with a warmer climate. B. burgdorferi was identified at 13 I. scapularis–positive sites, but infection prevalence in ticks and animal hosts was low. Low infection prevalence in ticks submitted in passive surveillance after 2004—from the tick-positive regions identified in active surveillance—coincided with an exponential increase in tick submissions during this time. MLST analysis suggested recent introduction of B. burgdorferi from the northeastern United States. Conclusions These data are consistent with I. scapularis ticks dispersed from the United States by migratory birds, founding populations where the climate is warmest, and then establishment of B. burgdorferi from the United States several years after I. scapularis have established. These observations provide vital information for public health to minimize the impact of LD in Canada.

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.

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.

Factors associated with preventive behaviors regarding Lyme disease in Canada and Switzerland: a comparative study

BackgroundLyme disease (LD) is a vector-borne disease that is endemic in many temperate countries, including Switzerland, and is currently emerging in Canada. This study compares the importance of knowledge, exposure and risk perception for the adoption of individual preventive measures, within and between two different populations, one that has been living in a LD endemic region for several decades, the Neuchâtel canton in Switzerland, and another where the disease is currently emerging, the Montérégie region in the province of Québec, Canada.MethodsA web-based survey was carried out in both study regions (814 respondents) in 2012. Comparative analysis of the levels of adoption of individual preventive measures was performed and multivariable logistic regression analyses were used to test and compare how knowledge, exposure and risk perception were associated with the adoption of selected measures in both regions and globally.ResultsIn Montérégie, the proportion of reported adoption of five of the most commonly recommended preventive measures varied from 6% for ‘applying acaricides on one’s property’ to 49% for ‘wearing protective clothing’, and in Neuchâtel, proportions ranged from 6% (acaricides) to 77% for ‘checking for ticks (tick check)’. Differences were found within gender, age groups and exposure status in both regions. The perceived efficacy of a given measure was the strongest factor associated with the adoption of three specific preventive behaviors for both regions: tick check, protective clothing and tick repellent. Risk perception and a high level of knowledge about LD were also significantly associated with some of these specific behaviors, but varied by region.ConclusionsThese results strongly suggest that social and contextual factors such as the epidemiological status of a region are important considerations to take into account when designing effective prevention campaigns for Lyme disease. It furthermore underlines the importance for public health authorities to better understand and monitor these factors in targeted populations in order to be able to implement preventive programs that are well adapted to a population and the epidemiological contexts therein.

From Lyme disease emergence to endemicity: a cross sectional comparative study of risk perceptions in different populations

BackgroundLyme disease (LD) is a tick-borne emerging disease in Canada that has been endemic in many temperate countries for decades. Currently, one of the main approaches for LD prevention is the promotion of individual-level preventive behaviors against ticks. Health behaviors are influenced by individual and social factors, one important of which is risk perception. This study aims to describe and compare risk perception of LD, within and between general populations and experts living in two different regions: the Neuchâtel canton in Switzerland, where LD is endemic, and the Montérégie region in Québec (Canada), where LD is emerging.MethodA web-based survey was conducted in both study regions (814 respondents) in 2012, and a questionnaire was administered to 16 experts. Comparative analyses of knowledge, risk exposure and different components of LD risk perception were performed. Multivariate analyses were used to calculate a global risk perception score and to identify determinants of risk perception in both regions.ResultsIn Montérégie, only 15% of the survey respondents had a good level of knowledge of LD compared to Neuchâtel where 51% of survey respondents had good levels of knowledge. In Montérégie, 24% of respondents perceived themselves as being at high or very high risk of contracting LD vs 54% in Neuchâtel; however, a higher percentage of respondents from this region believed that personal protection was simple to carry out (73% vs 58% in Montérégie). Based on the population surveys, almost all of the identified determinants of risk perception were different between both populations except for gender. A good level of knowledge, living in the risk zone and knowing someone who has had LD increased risk perception, while a high level of education and being 18–34 years of age decreased this perception. The majority of the studied components of risk perception were different between populations and their regional experts.ConclusionThis study suggests that risk perception of LD differs between populations and regional experts living in different epidemiological situations. Monitoring of knowledge and risk perception in local populations may help to better target LD communication efforts in accordance with population specific attributes thereby enhancing prevention efficacy.

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.

Adaptation and Evaluation of a Multi-Criteria Decision Analysis Model for Lyme Disease Prevention.

Designing preventive programs relevant to vector-borne diseases such as Lyme disease (LD) can be complex given the need to include multiple issues and perspectives into prioritizing public health actions. A multi-criteria decision aid (MCDA) model was previously used to rank interventions for LD prevention in Quebec, Canada, where the disease is emerging. The aim of the current study was to adapt and evaluate the decision model constructed in Quebec under a different epidemiological context, in Switzerland, where LD has been endemic for the last thirty years. The model adaptation was undertaken with a group of Swiss stakeholders using a participatory approach. The PROMETHEE method was used for multi-criteria analysis. Key elements and results of the MCDA model are described and contrasted with the Quebec model. All criteria and most interventions of the MCDA model developed for LD prevention in Quebec were directly transferable to the Swiss context. Four new decision criteria were added, and the list of proposed interventions was modified. Based on the overall group ranking, interventions targeting human populations were prioritized in the Swiss model, with the top ranked action being the implementation of a large communication campaign. The addition of criteria did not significantly alter the intervention rankings, but increased the capacity of the model to discriminate between highest and lowest ranked interventions. The current study suggests that beyond the specificity of the MCDA models developed for Quebec and Switzerland, their general structure captures the fundamental and common issues that characterize the complexity of vector-borne disease prevention. These results should encourage public health organizations to adapt, use and share MCDA models as an effective and functional approach to enable the integration of multiple perspectives and considerations in the prevention and control of complex public health issues such as Lyme disease or other vector-borne and zoonotic diseases.

Lyme Disease: Knowledge and Practices of Family Practitioners in Southern Quebec

As the range of the blacklegged tick (Ixodes scapularis) expands into southern Quebec, cases of Lyme disease – caused by Borrelia burgdorferi and transmitted by blacklegged ticks – are also expected to rise. The authors of this article aimed to compare the experience, knowledge and practices regarding Lyme disease of physicians in Montérégie, a region affected by Lyme disease, with phyisicians in other regions not yet affected by the disease.

Practices of Lyme disease diagnosis and treatment by general practitioners in Quebec, 2008–2015

BackgroundLyme disease (LD), a multisystem infection caused by the spirochete Borrelia burgdorferi sensu stricto (B. burgdorferi), is the most reported vector-borne disease in North America, and by 2020, 80% of the population in central and eastern Canada could live in LD risk areas. Among the key factors for minimising the impact of LD are the accurate diagnosis and appropriate management of patients bitten by ticks. In this study, the practices of Quebec general practitioners (GPs) on LD diagnosis and management of patients bitten by infected ticks are described.MethodsEight years (2008 to 2015) of retrospective demographic and clinical data on patients bitten by infected Ixodes scapularis (I. scapularis) ticks and on the management of suspected and confirmed LD cases by Quebec GPs were analysed.ResultsAmong 50 patients, all the antimicrobial treatments of LD clinical cases were appropriate according to current guidelines. However, more than half (62.8%) of erythema migrans (EM) were possibly misdiagnosed, 55.6%, (n = 27) of requested serologic tests were possibly unnecessary and the majority (96.5%, n = 57) of prophylactic antimicrobial treatments were not justified according to current guidelines.ConclusionsThese observations underline the importance for public health to enhance the knowledge of GPs where LD is emerging, to minimise the impact of the disease on patients and the financial burden on the health system.