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.

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.

Tick-borne encephalitis in the age of general mobility.

The 11th meeting of the International Scientific Working Group on Tick-borne Encephalitis (ISW-TBE) was conducted under the title of, "From childhood to golden age: increased mobility - increased risk of contracting TBE?" Participants from 26 countries, including the United States of America and China, presented reports on the latest developments and trends in local TBE cases, vaccination coverage and risk factors. In particular, the situation of children and the elderly (the "golden agers") was discussed. As the current evidence suggests, the location and extension of endemic areas for TBE have changed over the last few years, along with global warming and the shift of infected ticks to higher altitudes. The increased mobility of the human population adds to the heightened exposure; outdoor activities and international travel are on the rise also, and especially, amongst the 50+ generation, who are already per se at higher risk of disease manifestation, complications and case fatality. Most Europeans travel within Europe, often without sufficient awareness of endemic areas. Only high immunization rates can ensure low disease rates in the long run. To achieve this goal, public education is the sole effective approach for raising the level of awareness. Overall, the risk of any given person to contract TBE should not be regarded as a fixed entity, but rather it must be estimated individually, on the basis of knowledge of the TBE virus endemic areas and risk factors.

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.

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.

Studying the global distribution of infectious diseases using GIS and RS.

West Nile virus, severe acute respiratory syndrome and monkeypox are infectious diseases that have recently been introduced into areas far from their region of origin. The greatest risk of new diseases comes from zoonoses--pathogens that circulate among wild animals and are occasionally transferred to humans by intermediate invertebrate hosts or vectors that are sensitive to climatic conditions. Analytical tools that are based on geographical information systems and that can incorporate remotely sensed information about the environment offer the potential to define the limiting conditions for any disease in its native region for which there are at least some distribution data. The direction, intensity or likelihood of its spread to new regions could then be predicted, potentially allowing disease early-warning systems to be developed.

Mapping bovine tuberculosis in Great Britain using environmental data.

The incidence of bovine tuberculosis (BTB) is increasing in Great Britain, exacerbated by the temporary suspension of herd testing in 2001 for fear of spreading the much more contagious foot and mouth disease. The transmission pathways of BTB remain poorly understood. Current hypotheses suggest the disease is introduced into susceptible herds from a wildlife reservoir (principally the Eurasian Badger) and/or from cattle purchased from infected areas, while the role of climatic factors in transmission has generally been ignored. Here, we show how remotely sensed satellite data, which provide good indicators of a variety of climatic factors, can be used to describe the distribution of BTB in Great Britain in 1997, and suggest how such data could be used to produce BTB risk maps for the future.

Climate variability and malaria epidemics in the highlands of East Africa.

Malaria epidemics in the highlands of East Africa garner significant research attention, due, in part, to their proposed sensitivity to climate change. In a recent article, Zhou et al. claim that increases in climate variance, rather than simple increases in climate mean values, have had an important role in the resurgence of malaria epidemics in the East African highlands since the early 1980s. If proven, this would be an interesting result but we believe that the methods used do not test the hypothesis suggested.

A response to the aim of eradicating tsetse from Africa.

An ambitious plan to eradicate tsetse, and therefore tsetse-transmitted trypanosomiases, from Africa was launched at the 36th Organization of African Unity summit meeting (Togo, July 2000) in a bold attempt to re-focus attention on one of Africa's greatest scourges. This plan involves the use of the sterile insect technique to achieve final eradication in areas where the fly is suppressed by more conventional methods (such as traps and targets). In this article, the current aims of this project are questioned on historical, ecological, logistical and financial grounds.

Hot topic or hot air? Climate change and malaria resurgence in East African highlands.

Climate has a significant impact on malaria incidence and we have predicted that forecast climate changes might cause some modifications to the present global distribution of malaria close to its present boundaries. However, it is quite another matter to attribute recent resurgences of malaria in the highlands of East Africa to climate change. Analyses of malaria time-series at such sites have shown that malaria incidence has increased in the absence of co-varying changes in climate. We find the widespread increase in resistance of the malaria parasite to drugs and the decrease in vector control activities to be more likely driving forces behind the malaria resurgence.

An empirical quantitative framework for the seasonal population dynamics of the tick Ixodes ricinus.

The wide geographic and climatic range of the tick Ixodes ricinus, and the consequent marked variation in its seasonal population dynamics, have a direct impact on the transmission dynamics of the many pathogens vectored by this tick species. We use long-term observations on the seasonal abundance and fat contents (a marker of physiological ageing) of ticks, and contemporaneous microclimate at three field sites in the UK, to establish a simple quantitative framework for the phenology (i.e. seasonal cycle of development) of I. ricinus as a foundation for a generic population model. An hour-degree tick inter-stadial development model, driven by soil temperature and including diapause, predicts the recruitment (i.e. emergence from the previous stage) of a single cohort of each stage of ticks each year in the autumn. The timing of predicted emergence coincides exactly with the new appearance of high-fat nymphs and adults in the autumn. Thereafter, fat contents declined steadily until unfed ticks with very low energy reserves disappeared from the questing population within about 1 year from their recruitment. Very few newly emerged ticks were counted on the vegetation in the autumn, but they appeared in increasing numbers through the following spring. Larger ticks became active and subsequently left the questing population before smaller ones. Questing tick population dynamics are determined by seasonal patterns of tick behaviour, host-contact rates and mortality rates, superimposed on a basal phenology that is much less complex than has hitherto been portrayed.

Quantitative ecology of ticks as a basis for transmission models of tick-borne pathogens.

Tick population ecology is the basis of spatiotemporal variation in the risk of infection by tick-borne pathogens. The continental distribution of tick-borne encephalitis (TBE) in Europe is statistically associated with a specific pattern of the seasonal dynamics of Ixodes ricinus, and a particular characteristic of the seasonal land surface temperature profile. A tick population model would allow us to move from this statistical analysis to a biological, process-based model for TBE virus and the many other pathogens vectored by Ixodes spp. ticks in Europe and the United States. Long-term field data on I. ricinus are analyzed to provide empirical estimates of rates of the major demographic processes, development, questing, attachment to hosts, and mortality.

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.

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.

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.

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.