Is expert opinion enough? A critical assessment of the evidence for potential impacts of climate change on tick-borne diseases.

Before attributing cause and consequence to climate change, the precise patterns of change must be known. Ground records across much of Europe show a 1-2 °C rise in temperatures in 1989 with no significant rise since then. The timing and spatial uniformity of this pattern, relative to changes in the distribution and incidence of many vector-borne diseases, are sufficient to falsify most simple claims that climate change is the principal cause of disease emergence. Furthermore, age-specific increases in incidence indicate causes other than, or in addition to, climate change. Unfortunately, many public health professionals repeat the received wisdom that climate change is worsening the burden of indirectly transmitted infections; this 'expert opinion' soon becomes consensus dogma divorced from quantitative evidence. The pressing need is to gather appropriate data to test the simple concept that the composition and relative importance of disparate multifactorial factors, commonly integrated within a causal nexus, will inevitably vary with the geographical, cultural, socio-economical, wildlife, etc. context. The greatest impact of warming occurs at the geographical limits of current distributions, where low temperatures limit the hazard of infected vectors. Within core endemic regions, changing exposure of humans to this hazard, through changing socio-economic factors is evidently more important amongst both the poor and the wealthy.

Driving forces for changes in geographical distribution of Ixodes ricinus ticks in Europe.

Many factors are involved in determining the latitudinal and altitudinal spread of the important tick vector Ixodes ricinus (Acari: Ixodidae) in Europe, as well as in changes in the distribution within its prior endemic zones. This paper builds on published literature and unpublished expert opinion from the VBORNET network with the aim of reviewing the evidence for these changes in Europe and discusses the many climatic, ecological, landscape and anthropogenic drivers. These can be divided into those directly related to climatic change, contributing to an expansion in the tick's geographic range at extremes of altitude in central Europe, and at extremes of latitude in Scandinavia; those related to changes in the distribution of tick hosts, particularly roe deer and other cervids; other ecological changes such as habitat connectivity and changes in land management; and finally, anthropogenically induced changes. These factors are strongly interlinked and often not well quantified. Although a change in climate plays an important role in certain geographic regions, for much of Europe it is non-climatic factors that are becoming increasingly important. How we manage habitats on a landscape scale, and the changes in the distribution and abundance of tick hosts are important considerations during our assessment and management of the public health risks associated with ticks and tick-borne disease issues in 21(st) century Europe. Better understanding and mapping of the spread of I. ricinus (and changes in its abundance) is, however, essential to assess the risk of the spread of infections transmitted by this vector species. Enhanced tick surveillance with harmonized approaches for comparison of data enabling the follow-up of trends at EU level will improve the messages on risk related to tick-borne diseases to policy makers, other stake holders and to the general public.

Drivers, dynamics, and control of emerging vector-borne zoonotic diseases.

Emerging vector-borne diseases are an important issue in global health. Many vector-borne pathogens have appeared in new regions in the past two decades, while many endemic diseases have increased in incidence. Although introductions and emergence of endemic pathogens are often considered to be distinct processes, many endemic pathogens are actually spreading at a local scale coincident with habitat change. We draw attention to key differences between dynamics and disease burden that result from increased pathogen transmission after habitat change and after introduction into new regions. Local emergence is commonly driven by changes in human factors as much as by enhanced enzootic cycles, whereas pathogen invasion results from anthropogenic trade and travel where and when conditions (eg, hosts, vectors, and climate) are suitable for a pathogen. Once a pathogen is established, ecological factors related to vector characteristics can shape the evolutionary selective pressure and result in increased use of people as transmission hosts. We describe challenges inherent in the control of vector-borne zoonotic diseases and some emerging non-traditional strategies that could be effective in the long term.

A national case-control study identifies human socio-economic status and activities as risk factors for tick-borne encephalitis in Poland.

BACKGROUND: Tick-borne encephalitis (TBE) is endemic to Europe and medically highly significant. This study, focused on Poland, investigated individual risk factors for TBE symptomatic infection. METHODS AND FINDINGS: In a nation-wide population-based case-control study, of the 351 TBE cases reported to local health departments in Poland in 2009, 178 were included in the analysis. For controls, of 2704 subjects (matched to cases by age, sex, district of residence) selected at random from the national population register, two were interviewed for each case and a total of 327 were suitable for the analysis. Questionnaires yielded information on potential exposure to ticks during the six weeks (maximum incubation period) preceding disease onset in each case. Independent associations between disease and socio-economic factors and occupational or recreational exposure were assessed by conditional logistic regression, stratified according to residence in known endemic and non-endemic areas. Adjusted population attributable fractions (PAF) were computed for significant variables. In endemic areas, highest TBE risk was associated with spending ≥10 hours/week in mixed forests and harvesting forest foods (adjusted odds ratio 19.19 [95% CI: 1.72-214.32]; PAF 0.127 [0.064-0.193]), being unemployed (11.51 [2.84-46.59]; 0.109 [0.046-0.174]), or employed as a forester (8.96 [1.58-50.77]; 0.053 [0.011-0.100]) or non-specialized worker (5.39 [2.21-13.16]; 0.202 [0.090-0.282]). Other activities (swimming, camping and travel to non-endemic regions) reduced risk. Outside TBE endemic areas, risk was greater for those who spent ≥10 hours/week on recreation in mixed forests (7.18 [1.90-27.08]; 0.191 [0.065-0.304]) and visited known TBE endemic areas (4.65 [0.59-36.50]; 0.058 [-0.007-0.144]), while travel to other non-endemic areas reduced risk. CONCLUSIONS: These socio-economic factors and associated human activities identified as risk factors for symptomatic TBE in Poland are consistent with results from previous correlational studies across eastern Europe, and allow public health interventions to be targeted at particularly vulnerable sections of the population.

Transmission of tick-borne pathogens between co-feeding ticks: Milan Labuda's enduring paradigm.

During the 1990s, Milan Labuda's experimental results established a new paradigm for the study of tick-borne viruses that has since been strengthened by its demonstrated effectiveness in explaining the epidemiology of tick-borne encephalitis (TBE). This brief review summarizes the essential features of the transmission of tick-borne pathogens such as TBE virus. Leukocytes migrate between tick feeding sites, bearing infective virions and providing a transport route for the virus between co-feeding ticks independent of a systemic viraemia. Such tick-borne pathogens are thus transmitted from tick to tick via vertebrates; the ticks are the reservoirs as well as the vectors, while the vertebrate is the transient bridge. The aim is to bring the related but non-synonymous terms (co-feeding and non-systemic) to the attention of workers who use simple PCR screening to identify additional vertebrate reservoir hosts of vector-borne pathogens that are not in fact maintained in nature through systemic transmission.

Tick (Ixodes ricinus) abundance and seasonality at recreational sites in the UK: hazards in relation to fine-scale habitat types revealed by complementary sampling methods.

The seasonal risk to humans of picking up Ixodes ricinus ticks in different habitats at 3 recreational sites in the UK was assessed. A comprehensive range of vegetation types was sampled at 3-weekly intervals for 2 years, using standard blanket-dragging complemented by woollen leggings and square 'heel flags'. Ticks were found in all vegetation types sampled, including short grass close to car parks, but highest densities were consistently found in plots with trees present. Blankets picked up the greatest number of ticks, but heel flags provided important complementary counts of the immature stages in bracken plots; they showed clearly that the decline in tick numbers on blankets in early summer was due to the seasonal growth of vegetation that lifted the blanket clear of the typical questing height, but in reality ticks remained abundant through the summer. Leggings picked up only 11% of the total nymphs and 22% of total adults counted, but this still represented a significant hazard to humans. These results should prompt a greater awareness of the fine-scale distribution of this species in relation to human activities that determines the most likely zones of contact between humans and ticks. Risk communication may then be designed accordingly.

Frameworks for risk communication and disease management: the case of Lyme disease and countryside users.

Management of zoonotic disease is necessary if countryside users are to gain benefit rather than suffer harm from their activities, and to avoid disproportionate reaction to novel threats. We introduce a conceptual framework based on the pressure-state-response model with five broad responses to disease incidence. Influencing public behaviour is one response and requires risk communication based on an integration of knowledge about the disease with an understanding of how publics respond to precautionary advice. A second framework emphasizes how risk communication involves more than information provision and should address dimensions including points-of-intervention over time, place and audience. The frameworks are developed by reference to tick-borne Lyme borreliosis (also known as Lyme disease), for which informed precautionary behaviour is particularly relevant. Interventions to influence behaviour can be directed by knowledge of spatial and temporal variation of tick abundance, what constitutes risky behaviour, how people respond to information of varying content, and an understanding of the social practices related to countryside use. The frameworks clarify the response options and help identify who is responsible for risk communication. These aspects are not consistently understood, and may result in an underestimation of the role of land-based organizations in facilitating appropriate precautionary behaviour.

Economic downturn results in tick-borne disease upsurge.

BACKGROUND: The emergence of zoonoses is due both to changes in human activities and to changes in their natural wildlife cycles. One of the most significant vector-borne zoonoses in Europe, tick-borne encephalitis (TBE), doubled in incidence in 1993, largely as a consequence of the socio-economic transition from communism to capitalism and associated environmental changes. METHODS: To test the effect of the current economic recession, unemployment in 2009 and various socio-economic indices were compared to weather indices (derived from principal component analyses) as predictors for the change in TBE case numbers in 2009 relative to 2004-08, for 14 European countries. RESULTS: Greatest increases in TBE incidence occurred in Latvia, Lithuania and Poland (91, 79 and 45%, respectively). The weather was rejected as an explanatory variable. Indicators of high background levels of poverty, e.g. percent of household expenditure on food, were significant predictors. The increase in unemployment in 2009 relative to 2008 together with 'in-work risk of poverty' is the only case in which a multivariate model has a second significant term. CONCLUSION: Background socio-economic conditions determine susceptibility to risk of TBE, while increased unemployment triggered a sudden increase in risk. Mechanisms behind this result may include reduced resistance to infection through stress; reduced uptake of costly vaccination; and more exposure of people to infected ticks in their forest habitat as they make greater use of wild forest foods, especially in those countries, Lithuania and Poland, with major marketing opportunities in such products. Recognition of these risk factors could allow more effective protection through education and a vaccination programme targeted at the economically most vulnerable.

Host migration impacts on the phylogeography of Lyme Borreliosis spirochaete species in Europe.

The geographic patterns of transmission opportunities of vector-borne zoonoses are determined by a complex interplay between the migration patterns of the host and the vector. Here we examine the impact of host migration on the spread of a tick-borne zoonotic disease, using Lyme Borreliosis (LB) spirochaetal species in Europe. We demonstrate that the migration of the LB species is dependent on and limited by the migration of their respective hosts. We note that populations of Borrelia spp. associated with birds (Borrelia garinii and B. valaisiana) show limited geographic structuring between countries compared with those associated with small mammals (Borrelia afzelii), and we argue that this can be explained by higher rates of migration in avian hosts. We also show the presence of B. afzelii strains in England and, through the use of the multi-locus sequence analysis scheme, reveal that the strains are highly structured. This pattern in English sites is very different from that observed at the continental sites, and we propose that these may be recent introductions.

The arrival, establishment and spread of exotic diseases: patterns and predictions.

The impact of human activities on the principles and processes governing the arrival, establishment and spread of exotic pathogens is illustrated by vector-borne diseases such as malaria, dengue, chikungunya, West Nile, bluetongue and Crimean-Congo haemorrhagic fevers. Competent vectors, which are commonly already present in the areas, provide opportunities for infection by exotic pathogens that are introduced by travel and trade. At the same time, the correct combination of environmental conditions (both abiotic and biotic) makes many far-flung parts of the world latently and predictably, but differentially, permissive to persistent transmission cycles. Socioeconomic factors and nutritional status determine human exposure to disease and resistance to infection, respectively, so that disease incidence can vary independently of biological cycles.

Landscape predictors of tick-borne encephalitis in Latvia: land cover, land use, and land ownership.

Although the presence of tick-borne encephalitis (TBE) virus circulating in tick populations depends on large-scale patterns of climate, and the local density of infected ticks depends on the abundance of mammalian hosts, the risk of human infection depends on the access and use by human populations of tick-infested habitats, particularly forests, at the landscape level. We investigated the incidence of reported TBE cases in rural parishes (i.e., municipalities) in Latvia. The following major characteristics of parishes were considered: whether their environment is suitable for tick and tick-host populations (depending on land cover); whether the local human population is likely to enter the forest on a regular base (depending on land use); and whether the spatial distributions of these two aspects are likely to intersect, through access rules (as a function of land ownership). The results indicated that all three aspects are important in explaining and predicting the spatial distribution of TBE cases in the rural areas of Latvia. The concept of landscape is here given new depth by consideration of its physical structure, its use by human populations, and its accessibility as modulated by ownership.

To what extent has climate change contributed to the recent epidemiology of tick-borne diseases?

There is no doubt that all vector-borne diseases are very sensitive to climatic conditions. Many such diseases have shown marked increases in both distribution and incidence during the past few decades, just as human-induced climate change is thought to have exceeded random fluctuations. This coincidence has led to the general perception that climate change has driven disease emergence, but climate change is the inevitable backdrop for all recent events, without implying causality. Coincidence and causality can be disentangled using tick-borne encephalitis (TBE) as a test case, based on the excellent long-term data for this medically significant European disease system. Detailed analysis of climate records since 1970 has revealed abrupt temperature increases just prior to the dramatic upsurge in TBE incidence in many parts of central and eastern Europe. Furthermore, the seasonal patterns of this temperature change are such as might have favoured the transmission of TBE virus between co-feeding ticks. Nevertheless, the pattern of climate change is too uniform to explain the marked heterogeneity in the timing and degree of TBE upsurge, for example in different counties within each of the Baltic countries. Recent decreases as well as increases in TBE incidence must also be taken into account. Instead of a single cause, a network of interacting factors, acting synergistically but with differential force in space and time, would generate this epidemiological heterogeneity. From analysis of past and present events, it appears that human behavioural factors have played a more significant role than purely biological enzootic factors, although there is an explicit causal linkage from one to the other. This includes a range of abiotic and biotic environmental factors, together with human behaviour determined by socio-economic conditions. Many of the abrupt changes followed from the shift from planned to market economies with the fall of Soviet rule. Comparisons between eight countries have indeed revealed a remarkable correlation between poverty indicators and the relative degree of upsurge in TBE from 1993. Against this background of longer-term shifts in TBE incidence, sudden spikes in incidence appear to be due to exceptional weather conditions affecting people's behaviour, which have a differential impact depending on socio-economic factors. This new perspective may also help explain the epidemiology of Crimean-Congo haemorrhagic fever around the eastern Mediterranean region, including the current exceptional epidemic in Turkey.

Variable spikes in tick-borne encephalitis incidence in 2006 independent of variable tick abundance but related to weather.

BACKGROUND: The incidence of tick-borne encephalitis showed a dramatic spike in several countries in Europe in 2006, a year that was unusually cold in winter but unusually warm and dry in summer and autumn. In this study we examine the possible causes of the sudden increase in disease: more abundant infected ticks and/or increased exposure due to human behaviour, both in response to the weather. METHODS: For eight countries across Europe, field data on tick abundance for 2005-2007, collected monthly from a total of 41 sites, were analysed in relation to total annual and seasonal TBE incidence and temperature and rainfall conditions. RESULTS: The weather in 2006-2007 was exceptional compared with the previous two decades, but neither the very cold start to 2006, nor the very hot period from summer 2006 to late spring 2007 had any consistent impact on tick abundance. Nor was the TBE spike in 2006 related to changes in tick abundance. Countries varied in the degree of TBE spike despite similar weather patterns, and also in the degree to which seasonal variation in TBE incidence matched seasonal tick activity. CONCLUSION: The data suggest that the TBE spike was not due to weather-induced variation in tick population dynamics. An alternative explanation, supported by qualitative reports and some data, involves human behavioural responses to weather favourable for outdoor recreational activities, including wild mushroom and berry harvest, differentially influenced by national cultural practices and economic constraints.

Tick-borne encephalitis virus, ticks and humans: short-term and long-term dynamics.

PURPOSE OF REVIEW: Much public health concern and scientific interest has been kindled by significant increases in incidence of tick-borne encephalitis over the past 1-2 decades. It is the most important vector-borne disease of humans in Europe, for which excellent long-term data allow robust quantitative analyses. RECENT FINDINGS: Despite the increasing tendency to attribute all increases in vector-borne diseases to climate change, there is no convincing evidence that the appearance of new foci in Sweden, Switzerland, France and Germany during this century, or the upsurge in cases within well recognized endemic regions, is due to the recorded minor extensions of infectious ticks into higher altitudes and latitudes and into winter periods, in response to warmer conditions. Rather, there is now good evidence of greater human exposure to infected ticks through altered socioeconomic circumstances (in addition to higher densities of tick-feeding deer--not reviewed here), so far best quantified for Central and Eastern Europe. SUMMARY: Increased awareness of tick-borne encephalitis and understanding of the changing risk factors, including the role of human behaviour, will ensure better personal protection against infection, including vaccination and avoidance of high-risk activities.

Behavioural responses to perceived risk of tick-borne encephalitis: vaccination and avoidance in the Baltics and Slovenia.

Tick-borne encephalitis (TBE) incidence increased markedly in the Baltics and Slovenia in the early 1990s, but then declined again in some places. Our analyses of temporal and spatial data on TBE incidence and vaccination revealed that over 1970-2005 up-take of vaccination varied in both time and space according to incidence, i.e. was apparently responsive to perceived risk. Since 1999, however, decreases in incidence in many counties within each country have far exceeded vaccination rates or immunity through natural exposure, and in Latvia and Lithuania these changes are correlated with previous incidence. Survey data on human activities in Latvia revealed that people in socio-economic groups whose behaviour put them at highest risk of exposure to ticks in forests, including people with lower education and lowest incomes, are least likely to be vaccinated. We conclude that risk avoidance through changing human behaviour has driven incidence-dependent decreases in TBE infection, but targeted vaccination campaigns could provide more secure protection.

Tick-borne encephalitis incidence in Central and Eastern Europe: consequences of political transition.

The variable, often dramatic, upsurge in tick-borne encephalitis in Central and Eastern Europe can best be understood as the result of a multi-factorial system of causes, including abiotic and biotic environmental changes, and human behaviour determined by socio-economic conditions. Many of these stem from the political transition with the end of Soviet rule.

Socio-economic factors in the differential upsurge of tick-borne encephalitis in Central and Eastern Europe.

Tick-borne encephalitis (TBE), the most serious widespread vector-borne disease of humans in Europe, increased from 2- to 30-fold in many Central and Eastern European countries from 1992 to 1993, coinciding with independence from Soviet rule. Unemployment and low income have been shown in Latvia to be statistically associated with high-risk behaviour involving harvest of wild foods from tick-infested forests, and also with not being vaccinated against TBE. Archival data for 1970--2005 record major changes in the agricultural and industrial sectors, and consequent changes in the abiotic and biotic environment and socio-economic conditions, which could have increased the abundance of infected ticks and the contact of humans with those ticks. For example, abandoned agricultural fields became suitable for rodent transmission hosts; use of pesticides and emissions of atmospheric industrial pollutants plummeted; wildlife hosts for ticks increased; tick populations appear to have responded; unemployment and inequality increased in all countries. These factors, by acting synergistically but differentially between and within each country, can explain the marked spatio-temporal heterogeneities in TBE epidemiology better than can climate change alone, which is too uniform across wide areas. Different degrees of socio-economic upheaval caused by political transition in Estonia, Latvia, Lithuania, Slovenia and the Czech Republic can apparently explain the marked variation in TBE upsurge. Causal linkage between national socio-economic conditions and epidemiology is strongly indicated by striking correlations across eight countries between the degree of upsurge of TBE and both poverty and household expenditure on food (R2 = 0.533 and 0.716, respectively).

Climate change cannot explain the upsurge of tick-borne encephalitis in the Baltics.

BACKGROUND: Pathogens transmitted by ticks cause human disease on a greater scale than any other vector-borne infections in Europe, and have increased dramatically over the past 2-3 decades. Reliable records of tick-borne encephalitis (TBE) since 1970 show an especially sharp upsurge in cases in Eastern Europe coincident with the end of Soviet rule, including the three Baltic countries, Estonia, Latvia and Lithuania, where national incidence increased from 1992 to 1993 by 64, 175 and 1,065%, respectively. At the county level within each country, however, the timing and degree of increase showed marked heterogeneity. Climate has also changed over this period, prompting an almost universal assumption of causality. For the first time, we analyse climate and TBE epidemiology at sufficiently fine spatial and temporal resolution to question this assumption. METHODOLOGY/PRINCIPAL FINDING: Detailed analysis of instrumental records of climate has revealed a significant step increase in spring-time daily maximum temperatures in 1989. The seasonal timing and precise level of this warming were indeed such as could promote the transmission of TBE virus between larval and nymphal ticks co-feeding on rodents. These changes in climate, however, are virtually uniform across the Baltic region and cannot therefore explain the marked spatio-temporal heterogeneity in TBE epidemiology. CONCLUSIONS/SIGNIFICANCE: Instead, it is proposed that climate is just one of many different types of factors, many arising from the socio-economic transition associated with the end of Soviet rule, that have acted synergistically to increase both the abundance of infected ticks and the exposure of humans to these ticks. Understanding the precise differential contribution of each factor as a cause of the observed epidemiological heterogeneity will help direct control strategies.