Persistence of Pathogens with Short Infectious Periods in Seasonal Tick Populations: The Relative Importance of Three Transmission Routes

BACKGROUND: The flaviviruses causing tick-borne encephalitis (TBE) persist at low but consistent levels in tick populations, despite short infectious periods in their mammalian hosts and transmission periods constrained by distinctly seasonal tick life cycles. In addition to systemic and vertical transmission, cofeeding transmission has been proposed as an important route for the persistence of TBE-causing viruses. Because cofeeding transmission requires ticks to feed simultaneously, the timing of tick activity may be critical to pathogen persistence. Existing models of tick-borne diseases do not incorporate all transmission routes and tick seasonality. Our aim is to evaluate the influence of seasonality on the relative importance of different transmission routes by using a comprehensive mathematical model. METHODOLOGY/PRINCIPAL FINDINGS: We developed a stage-structured population model that includes tick seasonality and evaluated the relative importance of the transmission routes for pathogens with short infectious periods, in particular Powassan virus (POWV) and the related "deer tick virus," emergent encephalitis-causing flaviviruses in North America. We used the next generation matrix method to calculate the basic reproductive ratio and performed elasticity analyses. We confirmed that cofeeding transmission is critically important for such pathogens to persist in seasonal tick populations over the reasonable range of parameter values. At higher but still plausible rates of vertical transmission, our model suggests that vertical transmission can strongly enhance pathogen prevalence when it operates in combination with cofeeding transmission. CONCLUSIONS/SIGNIFICANCE: Our results demonstrate that the consistent prevalence of POWV observed in tick populations could be maintained by a combination of low vertical, intermediate cofeeding and high systemic transmission rates. When vertical transmission is weak, nymphal ticks support integral parts of the transmission cycle that are critical for maintaining the pathogen. We also extended the model to pathogens that cause chronic infections in hosts and found that cofeeding transmission could contribute to elevating prevalence even in these systems. Therefore, the common assumption that cofeeding transmission is not relevant in models of chronic host infection, such as Lyme disease, could lead to underestimating pathogen prevalence

Economic downturn results in tick-borne disease upsurge

<p>Abstract</p> <p>Background</p> <p>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.</p> <p>Methods</p> <p>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.</p> <p>Results</p> <p>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.</p> <p>Conclusion</p> <p>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.</p

Multi-source analysis reveals latitudinal and altitudinal shifts in range of Ixodes ricinus at its northern distribution limit

<p>Abstract</p> <p>Background</p> <p>There is increasing evidence for a latitudinal and altitudinal shift in the distribution range of <it>Ixodes ricinus</it>. The reported incidence of tick-borne disease in humans is on the rise in many European countries and has raised political concern and attracted media attention. It is disputed which factors are responsible for these trends, though many ascribe shifts in distribution range to climate changes. Any possible climate effect would be most easily noticeable close to the tick's geographical distribution limits. In Norway- being the northern limit of this species in Europe- no documentation of changes in range has been published. The objectives of this study were to describe the distribution of <it>I. ricinus </it>in Norway and to evaluate if any range shifts have occurred relative to historical descriptions.</p> <p>Methods</p> <p>Multiple data sources - such as tick-sighting reports from veterinarians, hunters, and the general public - and surveillance of human and animal tick-borne diseases were compared to describe the present distribution of <it>I. ricinus </it>in Norway. Correlation between data sources and visual comparison of maps revealed spatial consistency. In order to identify the main spatial pattern of tick abundance, a principal component analysis (PCA) was used to obtain a weighted mean of four data sources. The weighted mean explained 67% of the variation of the data sources covering Norway's 430 municipalities and was used to depict the present distribution of <it>I. ricinus</it>. To evaluate if any geographical range shift has occurred in recent decades, the present distribution was compared to historical data from 1943 and 1983.</p> <p>Results</p> <p>Tick-borne disease and/or observations of <it>I. ricinus </it>was reported in municipalities up to an altitude of 583 metres above sea level (MASL) and is now present in coastal municipalities north to approximately 69°N.</p> <p>Conclusion</p> <p><it>I. ricinus </it>is currently found further north and at higher altitudes than described in historical records. The approach used in this study, a multi-source analysis, proved useful to assess alterations in tick distribution.</p

Factors affecting patterns of tick parasitism on forest rodents in tick-borne encephalitis risk areas, Germany

Identifying factors affecting individual vector burdens is essential for understanding infectious disease systems. Drawing upon data of a rodent monitoring programme conducted in nine different forest patches in southern Hesse, Germany, we developed models which predict tick (Ixodes spp. and Dermacentor spp.) burdens on two rodent species Apodemus flavicollis and Myodes glareolus. Models for the two rodent species were broadly similar but differed in some aspects. Patterns of Ixodes spp. burdens were influenced by extrinsic factors such as season, unexplained spatial variation (both species), relative humidity and vegetation cover (A. flavicollis). We found support for the ‘body mass’ (tick burdens increase with body mass/age) and for the ‘dilution’ hypothesis (tick burdens decline with increasing rodent densities) and little support for the ‘sex-bias’ hypothesis (both species). Surprisingly, roe deer densities were not correlated with larvae counts on rodents. Factors influencing the mean burden did not significantly explain the observed dispersion of tick counts. Co-feeding aggregations, which are essential for tick-borne disease transmission, were mainly found in A. flavicollis of high body mass trapped in areas with fast increase in spring temperatures. Locally, Dermacentor spp. appears to be an important parasite on A. flavicollis and M. glareolus. Dermacentor spp. was rather confined to areas with higher average temperatures during the vegetation period. Nymphs of Dermacentor spp. mainly fed on M. glareolus and were seldom found on A. flavicollis. Whereas Ixodes spp. is the dominant tick genus in woodlands of our study area, the distribution and epidemiological role of Dermacentor spp. should be monitored closely

Abundance estimation of Ixodes ticks (Acari: Ixodidae) on roe deer (Capreolus capreolus)

Despite the importance of roe deer as a host for Ixodes ticks in central Europe, estimates of total tick burden on roe deer are not available to date. We aimed at providing (1) estimates of life stage and sex specific (larvae, nymphs, males and females, hereafter referred to as tick life stages) total Ixodes burden and (2) equations which can be used to predict the total life stage burden by counting the life stage on a selected body area. Within a period of 1½ years, we conducted whole body counts of ticks from 80 hunter-killed roe deer originating from a beech dominated forest area in central Germany. Averaged over the entire study period (winter 2007–summer 2009), the mean tick burden per roe deer was 64.5 (SE ± 10.6). Nymphs were the most numerous tick life stage per roe deer (23.9 ± 3.2), followed by females (21.4 ± 3.5), larvae (10.8 ± 4.2) and males (8.4 ± 1.5). The individual tick burden was highly aggregated (k = 0.46); levels of aggregation were highest in larvae (k = 0.08), followed by males (k = 0.40), females (k = 0.49) and nymphs (k = 0.71). To predict total life stage specific burdens based on counts on selected body parts, we provide linear equations. For estimating larvae abundance on the entire roe deer, counts can be restricted to the front legs. Tick counts restricted to the head are sufficient to estimate total nymph burden and counts on the neck are appropriate for estimating adult ticks (females and males). In order to estimate the combined tick burden, tick counts on the head can be used for extrapolation. The presented linear models are highly significant and explain 84.1, 77.3, 90.5, 91.3, and 65.3% (adjusted R2) of the observed variance, respectively. Thus, these models offer a robust basis for rapid tick abundance assessment. This can be useful for studies aiming at estimating effects of abiotic and biotic factors on tick abundance, modelling tick population dynamics, modelling tick-borne pathogen transmission dynamics or assessing the efficacy of acaricides

Attachment site selection of ticks on roe deer, Capreolus capreolus

The spatio-temporal attachment site patterns of ticks feeding on their hosts can be of significance if co-feeding transmission (i.e. from tick to tick without a systemic infection of the host) of pathogens affects the persistence of a given disease. Using tick infestation data on roe deer, we analysed preferred attachment sites and niche width of Ixodes ticks (larvae, nymphs, males, females) and investigated the degree of inter- and intrastadial aggregation. The different development stages showed rather consistent attachment site patterns and relative narrow feeding site niches. Larvae were mostly found on the head and on the front legs of roe deer, nymphs reached highest densities on the head and highest adult densities were found on the neck of roe deer. The tick stages feeding (larvae, nymphs, females) on roe deer showed high degrees of intrastadial spatial aggregation, whereas males did not. Male ticks showed large feeding site overlap with female ticks. Feeding site overlap between larval-female and larval-nymphal ticks did occur especially during the months May–August on the head and front legs of roe deer and might allow pathogen transmission via co-feeding. Tick density, niche width and niche overlap on roe deer are mainly affected by seasonality, reflecting seasonal activity and abundance patterns of ticks. Since different tick development stages occur spatially and temporally clustered on roe deer, transmission experiments of tick-borne pathogens are urgently needed

Borrelia burgdorferi sensu lato in Ixodes ricinus ticks collected from migratory birds in Southern Norway

<p>Abstract</p> <p>Background</p> <p><it>Borrelia burgdorferi </it>sensu lato (s.l.) are the causative agent for Lyme borreliosis (LB), the most common tick-borne disease in the northern hemisphere. Birds are considered important in the global dispersal of ticks and tick-borne pathogens through their migration. The present study is the first description of <it>B. burgdorferi </it>prevalence and genotypes in <it>Ixodes ricinus </it>ticks feeding on birds during spring and autumn migration in Norway.</p> <p>Methods</p> <p>6538 migratory birds were captured and examined for ticks at Lista Bird Observatory during the spring and the autumn migration in 2008. 822 immature <it>I. ricinus </it>ticks were collected from 215 infested birds. Ticks were investigated for infection with <it>B. burgdorferi </it>s.l. by real-time PCR amplification of the 16S rRNA gene, and <it>B. burgdorferi </it>s.l. were thereafter genotyped by melting curve analysis after real-time PCR amplification of the <it>hbb </it>gene, or by direct sequencing of the PCR amplicon generated from the <it>rrs </it>(16S)-<it>rrl </it>(23S) intergenetic spacer.</p> <p>Results</p> <p><it>B. burgdorferi </it>s.l. were detected in 4.4% of the ticks. The most prevalent <it>B. burgdorferi </it>genospecies identified were <it>B. garinii </it>(77.8%), followed by <it>B.valaisiana </it>(11.1%), <it>B. afzelii </it>(8.3%) and <it>B. burgdorferi </it>sensu stricto (2.8%).</p> <p>Conclusion</p> <p>Infection rate in ticks and genospecies composition were similar in spring and autumn migration, however, the prevalence of ticks on birds was higher during spring migration. The study supports the notion that birds are important in the dispersal of ticks, and that they may be partly responsible for the heterogeneous distribution of <it>B. burgdorferi </it>s.l. in Europe.</p

Surveillance of Arthropod Vector-Borne Infectious Diseases Using Remote Sensing Techniques: A Review

Epidemiologists are adopting new remote sensing techniques to study a variety of vector-borne diseases. Associations between satellite-derived environmental variables such as temperature, humidity, and land cover type and vector density are used to identify and characterize vector habitats. The convergence of factors such as the availability of multi-temporal satellite data and georeferenced epidemiological data, collaboration between remote sensing scientists and biologists, and the availability of sophisticated, statistical geographic information system and image processing algorithms in a desktop environment creates a fertile research environment. The use of remote sensing techniques to map vector-borne diseases has evolved significantly over the past 25 years. In this paper, we review the status of remote sensing studies of arthropod vector-borne diseases due to mosquitoes, ticks, blackflies, tsetse flies, and sandflies, which are responsible for the majority of vector-borne diseases in the world. Examples of simple image classification techniques that associate land use and land cover types with vector habitats, as well as complex statistical models that link satellite-derived multi-temporal meteorological observations with vector biology and abundance, are discussed here. Future improvements in remote sensing applications in epidemiology are also discussed