Surveillance of Ixodes ricinus ticks (Acari: Ixodidae) in Iceland

Background: Ixodes ricinus is a three-host tick, a principal vector of Borrelia burgdorferi (s.l.) and one of the main vectors of tick-borne encephalitis (TBE) virus. Iceland is located in the North Atlantic Ocean with subpolar oceanic climate. During the past 3–4 decades, average temperature has increased, supporting more favourable conditions for ticks. Reports of I. ricinus have increased in recent years. If these ticks were able to establish in a changing climate, Iceland may face new threats posed by tick-borne diseases. Methods: Active field surveillance by tick flagging was conducted at 111 sites around Iceland from August 2015 to September 2016. Longworth mammal traps were used to trap Apodemus sylvaticus in southwestern and southern Iceland. Surveillance on tick importation by migratory birds was conducted in southeastern Iceland, using bird nets and a Heligoland trap. Vulpes lagopus carcasses from all regions of the country were inspected for ticks. In addition, existing and new passive surveillance data from two institutes have been merged and are presented. Continental probability of presence models were produced. Boosted Regression Trees spatial modelling methods and its predictions were assessed against reported presence. Results: By field sampling 26 questing I. ricinus ticks (7 males, 3 females and 16 nymphs) were collected from vegetation from three locations in southern and southeastern Iceland. Four ticks were found on migratory birds at their arrival in May 2016. A total of 52 A. sylvaticus were live-trapped but no ticks were found nor on 315 V. lagopus carcasses. Passive surveillance data collected since 1976, reports further 214 I. ricinus ticks from 202 records, with an increase of submissions in recent years. The continental probability of presence model correctly predicts approximately 75% of the recorded presences, but fails to predict a fairly specific category of recorded presence in areas where the records are probably opportunistic and not likely to lead to establishment. Conclusions: To the best of our knowledge, this study represents the first finding of questing I. ricinus ticks in Iceland. The species could possibly be established locally in Iceland in low abundance, although no questing larvae have yet been detected to confirm established populations. Submitted tick records have increased recently, which may reflect an increase in exposure, or in interest in ticks. Furthermore, the amount of records on dogs, cats and humans indicate that ticks were acquired locally, presenting a local biting risk. Tick findings on migratory birds highlight a possible route of importation. Obtaining questing larvae is now a priority to confirm that I. ricinus populations are established in Iceland. Further surveys on wild mammals (e.g. Rangifer tarandus), livestock and migratory birds are recommended to better understand their role as potential hosts for I. ricinus.Work was carried out under VectorNet, a European network for sharing data on the geographic distribution of arthropod vectors, transmitting human and animal disease agents (framework contract OC/EFSA/AHAW/2013/02-FWC1) funded by the European Food Safety Authority (EFSA) and the European Centre for Disease prevention and Control (ECDC). JM is also partly funded by the National Institute for Health Research Health Protection Research Unit (NIHR HPRU) in Environmental Change and Health at the London School of Hygiene & Tropical Medicine in partnership with Public Health England (PHE), and in collaboration with the University of Exeter, University College London, and the Met Office; and partly funded by the NIHR HPRU on Emerging Infections and Zoonoses at the University of Liverpool in partnership with PHE and Liverpool School of Tropical Medicine.Peer Reviewe

Can interventions that aim to decrease Lyme disease hazard at non-domestic sites be effective without negatively affecting ecosystem health? A systematic review protocol

Background Lyme disease (LD) is the most commonly reported, broadly distributed vector-borne disease of the northern temperate zone. It is transmitted by ticks and, if untreated, can cause skin, cardiac, nervous system and musculoskeletal disease. The distribution and incidence of LD is increasing across much of North America and Western Europe. Interventions to decrease exposure to LD hazard by encouraging behavioural change have low acceptance in high risk groups, and a safe, effective human LD vaccine is not presently available. As a result, habitat level interventions to decrease LD hazard itself (i.e. levels of infected ticks) have been proposed. However, some interventions may potentially negatively affect ecosystem health, and consequentially be neither desirable, nor politically feasible. This systematic review will catalogue interventions that aim to reduce LD hazard at non-domestic sites, and examine the evidence supporting those which are unlikely to negatively affect ecosystem health. Methods The review will be carried out in two steps. First, a screening and cataloguing stage will be conducted to identify and characterise interventions to decrease LD hazard at non-domestic sites. Secondly, the subset of interventions identified during cataloguing as unlikely to negatively affect ecosystem health will be investigated. In the screening and cataloguing step literature will be collected through database searching using pre-chosen search strings, hand-searching key journals and reviewing the websites of public health bodies. Further references will be identified by contacting stakeholders and researchers. Article screening and assessment of the likely effects of interventions on ecosystem health will be carried out independently by two reviewers. A third reviewer will be consulted if disagreements arise. The cataloguing step results will be presented in tables. Study quality will then be assessed independently by two reviewers, using adapted versions of established tools developed in healthcare research. These results will be presented in a narrative synthesis alongside tables. Though a full meta-analysis is not expected to be possible, if sub-groups of studies are sufficiently similar to compare, a partial meta-analysis will be carried out

Decelerating Spread of West Nile Virus by Percolation in a Heterogeneous Urban Landscape

Vector-borne diseases are emerging and re-emerging in urban environments throughout the world, presenting an increasing challenge to human health and a major obstacle to development. Currently, more than half of the global population is concentrated in urban environments, which are highly heterogeneous in the extent, degree, and distribution of environmental modifications. Because the prevalence of vector-borne pathogens is so closely coupled to the ecologies of vector and host species, this heterogeneity has the potential to significantly alter the dynamical systems through which pathogens propagate, and also thereby affect the epidemiological patterns of disease at multiple spatial scales. One such pattern is the speed of spread. Whereas standard models hold that pathogens spread as waves with constant or increasing speed, we hypothesized that heterogeneity in urban environments would cause decelerating travelling waves in incipient epidemics. To test this hypothesis, we analysed data on the spread of West Nile virus (WNV) in New York City (NYC), the 1999 epicentre of the North American pandemic, during annual epizootics from 2000–2008. These data show evidence of deceleration in all years studied, consistent with our hypothesis. To further explain these patterns, we developed a spatial model for vector-borne disease transmission in a heterogeneous environment. An emergent property of this model is that deceleration occurs only in the vicinity of a critical point. Geostatistical analysis suggests that NYC may be on the edge of this criticality. Together, these analyses provide the first evidence for the endogenous generation of decelerating travelling waves in an emerging infectious disease. Since the reported deceleration results from the heterogeneity of the environment through which the pathogen percolates, our findings suggest that targeting control at key sites could efficiently prevent pathogen spread to remote susceptible areas or even halt epidemics

Habitat properties are key drivers of Borrelia burgdorferi (s.l.) prevalence in Ixodes ricinus populations of deciduous forest fragments

Background: The tick Ixodes ricinus has considerable impact on the health of humans and other terrestrial animals because it transmits several tick-borne pathogens (TBPs) such as B. burgdorferi (sensu lato), which causes Lyme borreliosis (LB). Small forest patches of agricultural landscapes provide many ecosystem services and also the disservice of LB risk. Biotic interactions and environmental filtering shape tick host communities distinctively between specific regions of Europe, which makes evaluating the dilution effect hypothesis and its influence across various scales challenging. Latitude, macroclimate, landscape and habitat properties drive both hosts and ticks and are comparable metrics across Europe. Therefore, we instead assess these environmental drivers as indicators and determine their respective roles for the prevalence of B. burgdorferi in I. ricinus. Methods: We sampled I. ricinus and measured environmental properties of macroclimate, landscape and habitat quality of forest patches in agricultural landscapes along a European macroclimatic gradient. We used linear mixed models to determine significant drivers and their relative importance for nymphal and adult B. burgdorferi prevalence. We suggest a new prevalence index, which is pool-size independent. Results: During summer months, our prevalence index varied between 0 and 0.4 per forest patch, indicating a low to moderate disservice. Habitat properties exerted a fourfold larger influence on B. burgdorferi prevalence than macroclimate and landscape properties combined. Increasingly available ecotone habitat of focal forest patches diluted and edge density at landscape scale amplified B. burgdorferi prevalence. Indicators of habitat attractiveness for tick hosts (food resources and shelter) were the most important predictors within habitat patches. More diverse and abundant macro- and microhabitat had a diluting effect, as it presumably diversifies the niches for tick-hosts and decreases the probability of contact between ticks and their hosts and hence the transmission likelihood.[br/] Conclusions: Diluting effects of more diverse habitat patches would pose another reason to maintain or restore high biodiversity in forest patches of rural landscapes. We suggest classifying habitat patches by their regulating services as dilution and amplification habitat, which predominantly either decrease or increase B. burgdorferi prevalence at local and landscape scale and hence LB risk. Particular emphasis on promoting LB-diluting properties should be put on the management of those habitats that are frequently used by humans. In the light of these findings, climate change may be of little concern for LB risk at local scales, but this should be evaluated further

An updated meta-analysis of the distribution and prevalence of Borrelia burgdorferi s.l. in ticks in Europe

We updated a previous meta-analysis of the reported prevalence of Borrelia burgdorferi s.l. (Bb) in questing nymphs of Ixodes ricinus with literature from January 2010-June 2017. This resulted in 195 new papers providing the prevalence of Bb for 926 georeferenced records. Previously obtained geo-referenced data (878 records, years 2000-2010) were appended for modelling. The complete dataset contains data from 82,004 questing nymphs, resulting in 558 records of B. afzelii, 404 of B. burgdorferi s.s. (only 80 after the year 2010), 552 of B. garinii, 78 of B. lusitaniae, 61 of B. spielmanii, and 373 of B. valaisiana. The most commonly reported species are B. afzelii, B. garinii and B. valaisiana largely overlapping across Europe and their prevalence is associated with portions of the environmental niche. Highest prevalence occurs in areas of 280º-290º (Kelvin) of mean annual temperature experiencing a small amplitude, steady spring slope, and high mean values of and a moderate spring rise of vegetation vigor. Low prevalence occurs in sites with low and a noteworthy annual amplitude of temperature and NDVI (colder areas with abrupt annual changes of vegetation). We trained a neural network for predicting occurrence and prevalence, providing a correct classification rate of 89.5%. These results confirm the association of prevalence of the three most commonly reported species of Bb in Europe to parts of the environmental niche and provides a statistically tractable framework for analyzing trends under scenarios of climate change

Environmental drivers of Ixodes ricinus abundance in forest fragments of rural European landscapes

Background: The castor bean tick (Ixodes ricinus) transmits infectious diseases such as Lyme borreliosis, which constitutes an important ecosystem disservice. Despite many local studies, a comprehensive understanding of the key drivers of tick abundance at the continental scale is still lacking. We analyze a large set of environmental factors as potential drivers of I. ricinus abundance. Our multi-scale study was carried out in deciduous forest fragments dispersed within two contrasting rural landscapes of eight regions, along a macroclimatic gradient stretching from southern France to central Sweden and Estonia. We surveyed the abundance of I. ricinus, plant community composition, forest structure and soil properties and compiled data on landscape structure, macroclimate and habitat properties. We used linear mixed models to analyze patterns and derived the relative importance of the significant drivers. Results: Many drivers had, on their own, either a moderate or small explanatory value for the abundance of I. ricinus, but combined they explained a substantial part of variation. This emphasizes the complex ecology of I. ricinus and the relevance of environmental factors for tick abundance. Macroclimate only explained a small fraction of variation, while properties of macro- and microhabitat, which buffer macroclimate, had a considerable impact on tick abundance. The amount of forest and the composition of the surrounding rural landscape were additionally important drivers of tick abundance. Functional (dispersules) and structural (density of tree and shrub layers) properties of the habitat patch played an important role. Various diversity metrics had only a small relative importance. Ontogenetic tick stages showed pronounced differences in their response. The abundance of nymphs and adults is explained by the preceding stage with a positive relationship, indicating a cumulative effect of drivers. Conclusions: Our findings suggest that the ecosystem disservices of tick-borne diseases, via the abundance of ticks, strongly depends on habitat properties and thus on how humans manage ecosystems from the scale of the microhabitat to the landscape. This study stresses the need to further evaluate the interaction between climate change and ecosystem management on I. ricinus abundance