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

BACKGROUND: The bacteria of the group Borrelia burgdorferi s.l. are the etiological agents of Lyme borreliosis in humans, transmitted by bites of ticks. Improvement of control measures requires a solid framework of the environmental traits driving its prevalence in ticks. METHODS: We updated a previous meta-analysis of the reported prevalence of Borrelia burgdorferi s.l. in questing nymphs of Ixodes ricinus with a literature search from January 2010-June 2017. This resulted in 195 new papers providing the prevalence of Bb for 926 geo-referenced records. Previously obtained 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. We associated the records with explicit coordinates to environmental conditions and to a categorical definition of European landscapes (LANMAP2) looking for a precise definition of the environmental niche of the most reported species of the pathogen, using models based on different classification methods. RESULTS: The most commonly reported species are B. afzelii, B. garinii and B. valaisiana largely overlapping across Europe. Prevalence in ticks is associated with portions of the environmental niche. Highest prevalence occurs in areas of 280°-290° (Kelvin) of mean annual temperature experiencing a small amplitude, steady spring slope, together with high mean values and a moderate spring rise of vegetation vigor. Low prevalence occurs in sites with low and a noteworthy annual amplitude of temperature and the Normalized Difference Vegetation Index (colder areas with abrupt annual changes of vegetation). Models based on support vector machines provided a correct classification rate of the habitat and prevalence of 89.5%. These results confirm the association of prevalence of the three most commonly reported species of B. burgdorferi s.l. in Europe to parts of the environmental niche and provide a statistically tractable framework for analyzing trends under scenarios of climate change.

An Agenda for Research of Uncovered Epidemiological Patterns of Tick-Borne Pathogens Affecting Human Health.

The panorama of ticks and tick-borne pathogens (TBP) is complex due to the many interactions among vertebrates, vectors, and habitats, occurring at different scales. At a broad spatial range, climate and host availability regulate most tick processes, including questing activity, development, and survival. At a local scale, interactions are obscured by a high indeterminacy, making it arduous to record in field surveys. A solid modelling framework could translate the local/regional empirical findings into larger scales, shedding light on the processes governing the circulation of TBP. In this opinion paper, we advocate for a re-formulation of some paradigms in the research of these outstanding cycles of transmission. We propose revisiting concepts that faced criticisms or lacked solid support, together with the development of a conceptual scheme exploring the circulation of TBP under a range of conditions. We encourage (i) an adequate interpretation of the niche concept of both ticks and vertebrate/reservoir hosts interpreting the (a)biotic components that shape the tick's niche, (ii) an assessment of the role played by the communities of wild vertebrates on the circulation of pathogens, and (iii) the development of new approaches, based on state-of-the-art epidemiological concepts, to integrate findings and modelling efforts on TBP over large regions.

Passive collection of ticks in New Hampshire reveals species-specific patterns of distribution and activity.

Ticks and tick-borne diseases are increasing in the United States, including New Hampshire (NH). We report on the findings of an ongoing free crowdsourcing program spanning four years within NH. The date of tick's submission was recorded along with species, sex, stage, location they were collected (translated into latitude and longitude), the activity the individual was doing when the tick was found, and host species. A total of 14,252 ticks belonging to subclass Acari, family Ixodidae and genera Ixodes, Dermacentor, Amblyomma, and Haemaphysalis was recorded from the period 2018-2021 throughout NH. A total of 2,787 Ixodes scapularis and 1,041 Dermacentor variabilis, were tested for the presence of Borrelia sp. (Spirochaetales: Spirochaetaceae), B. burgdorferi sensu lato, B. miyamotoi, B. mayonii, Babesia microti (Piroplasmida: Babesiidae), Anaplasma phagocytophilum (Rickettsiales: Anaplasmataceae), Francisella tularensis (Thiotrichales: Francisellaceae), and Rickettsia rickettsii (Rickettsiales: Rickettsiaceae) by PCR. For the I. scapularis ticks tested, the pathogen prevalence was 37% B. burgdorferi s.l. 1% B. miyamotoi, 6% A. phagocytophilum, and 5% Ba. microti. Only one D. variabilis resulted positive to F. tularensis. We created state-wide maps informing the differences of ticks as detailed by administrative divisions. Dermacentor variabilis peaked in June and I. scapularis peaked in May and October. The most reported activity by people with tick encounters was while walking/hiking, and the least was biking. Using the reported distribution of both species of ticks, we modeled their climate suitability in the target territory. In NH, I. scapularis and D. variabilis have distinct patterns of emergence, abundance, and distribution. Tick prevention is important especially during April-August when both tick species are abundant and active.

Decontamination protocols affect the internal microbiota of ticks.

Studies on the microbiota of ticks have promoted hypotheses about the combined effects of the bacterial community, its functional contributions to the tick's physiology or probable competition effects with some tick-borne pathogens. However, knowledge on the origin of the microbiota of newly hatched larvae is missing. This study aimed to elucidate the source(s) of the microbiota in unfed tick larvae, addressing the composition of the "core microbiota" and the best ways to decontaminate eggs for microbiota studies. We applied laboratory degree bleach washes and/or ultraviolet light treatments on engorged Rhipicephalus australis females and/or their eggs. No significant effects of these treatments on the reproductive parameters of females and the hatching rates of eggs were observed. However, the different treatments did show striking effects on the composition of the microbiota. The results indicated that bleach washes disrupted the internal tick microbiota in females, implying that bleach may have entered the tick and subsequently affected the microbiota. Furthermore, the analyses of results demonstrated that the ovary is a main source of tick microbiota, while the contribution of Gené's organ (a part of the female reproductive system that secretes a protective wax coat onto tick eggs) or the male's spermatophore requires further investigation. Further studies are needed to identify best practice protocols for the decontamination of ticks for microbiota studies.

Is composition of vertebrates an indicator of the prevalence of tick-borne pathogens?

Communities of vertebrates tend to appear together under similar ranges of environmental features. This study explores whether an explicit combination of vertebrates and their contact rates with a tick vector might constitute an indicator of the prevalence of a pathogen in the quest for ticks at the western Palearctic scale. We asked how 'indicator' communities could be 'markers' of the actual infection rates of the tick in the field of two species of Borrelia (a bacterium transmitted by the tick Ixodes ricinus). We approached an unsupervised classification of the territory to obtain clusters on the grounds of abundance of each vertebrate and contact rates with the tick. Statistical models based on Neural Networks, Random Forest, Gradient Boosting, and AdaBoost were detect the best correlation between communities' composition and the prevalence of Borrelia afzelii and Borrelia gariniii in questing ticks. Both Gradient Boosting and AdaBoost produced the best results, predicting tick infection rates from the indicator communities. A ranking algorithm demonstrated that the prevalence of these bacteria in the tick is correlated with indicator communities of vertebrates on sites selected as a proof-of-concept. We acknowledge that our findings are supported by statistical outcomes, but they provide consistency for a framework that should be deeper explored at the large scale.

Scenes From Tick Physiology: Proteins of Sialome Talk About Their Biological Processes.

Ticks are blood-sucking parasites with different strategies of feeding depending on the tick family. The major families are Ixodidae or Argasidae, being slow or fast feeders, respectively. In the recent years, the advances in molecular sequencing techniques have enabled to gain knowledge about the proteome of the tick's salivary glands. But an holistic view of the biological processes underlying the expression of the sialome has been neglected. In this study we propose the use of standard biological processes as a tool to draw the physiology of the tick's salivary glands. We used published data on the sialome of Rhipicephalus sanguineus s.l. (Ixodidae) and Ornithodoros rostratus (Argasidae). A partial set of proteins obtained by these studies were used to define the biological process(es) in which proteins are involved. We used a directed network construction in which the nodes are proteins (source) and biological processes (target), separately for the low-level processes ("children") and the top-level ones ("parents"). We applied the method to feeding R. sanguineus at different time slices, and to different organs of O. rostratus. The network connects the proteins and the processes with a strength directly proportional to the transcript per millions of each protein. We used PageRank as a measure of the importance of each biological process. As suggested in previous studies, the sialome of unfed R. sanguineus express about 30% less biological processes than feeding ticks. Another decrease (25%) is noticed at the middle of the feeding and before detachment. However, top-level processes are deeply affected only at the onset of feeding, demonstrating a redundancy in the feeding. When ixodid-argasid are compared, large differences were observed: they do not share 91% of proteins, but share 90% of the biological processes. However, caution must be observed when examining these results. The hypothesis of different proteins linked to similar biological process(es) in both ticks is an extreme not confirmed in this study. Considering the limitations of this study, carried out with a selected set of proteins, we propose the networks of proteins of sialome linked to their biological processes as a tool aimed to explain the biological processes behind families of proteins.

Towards New Horizons: Climate Trends in Europe Increase the Environmental Suitability for Permanent Populations of Hyalomma marginatum (Ixodidae).

Ticks and tick-borne pathogens are changing their current distribution, presumably due to the impact of the climate trends. On a large scale, these trends are changing the environmental suitability of Hyalomma marginatum, the main vector of several pathogens affecting human health. We generated annual models of environmental suitability for the tick in the period 1970-2018, using harmonic regression-derived data of the daily maximum and minimum temperature, soil moisture and water vapor deficit. The results demonstrate an expansion of the suitable area in Mediterranean countries, southeast central Europe and south of the Balkans. Also, the models allowed us to interpret the impact of the ecological variables on these changes. We deduced that (i) maximum temperature was significant for all of the biogeographical categories, (ii) soil humidity has an influence in the Mediterranean climate areas, and (iii) the minimum temperature and deficit water vapor did not influence the environmental suitability of the species. The conclusions clearly show that climate change could create new areas in Europe with suitable climates for H. marginatum, while keeping its "historical" distribution in the Mediterranean. Therefore, it is necessary to further explore possible risk areas for H. marginatum and its associated pathogens.

Modelling the potential spread of Hyalomma marginatum ticks in Europe by migratory birds.

This study modelled the probability of introduction of Hyalomma marginatum into Europe by predicting the potential migratory routes of 28 bird species and the probability to carry immatures of the tick. Flyways were modelled as a spatio-temporal feature, at weekly intervals, using satellite-derived data of temperature and vegetal phenology, together with cost surfaces derived from speed and direction of the wind (years 2002-2018). The expected period of activity of tick immatures defined the probability of ticks being carried by birds along the modelled flyways. The probability of moulting of the engorged nymphs was modelled as a linear relationship of the daily sum of temperatures after tick introduction by birds. Positive probabilities of tick introduction extend the known northern range of permanent populations to central and western France, and large portions of central Europe. The flight of birds into an area and thence the risk of introduction of H. marginatum is very heterogeneous, with sites receiving "waves" of different bird species at diverse times of the year. Therefore, there is not a clear period of time for introduction, as it depends on the modelled behaviour of the bird species. The probability of introduction into Baltic and Nordic countries is small. We hypothesise that conditions of a warmer climate might support permanent populations of H. marginatum if a high number of immatures is introduced. Active surveys in risky territories, where the tick is not yet established, are advisable for rapid intervention.

Could climate trends disrupt the contact rates between Ixodes ricinus (Acari, Ixodidae) and the reservoirs of Borrelia burgdorferi s.l.?

This study addresses the modifications that future climate conditions could impose on the transmission cycles of Borrelia burgdorferi s.l. by the tick Ixodes ricinus in Europe. Tracking the distribution of foci of a zoonotic agent transmitted by vectors as climate change shapes its spatial niche is necessary to issue self-protection measures for the human population. We modeled the current distribution of the tick and its predicted contact rates with 18 species of vertebrates known to act as reservoirs of the pathogen. We approached an innovative way for estimating the possibility of permanent foci of Borrelia afzelii or Borrelia garinii tracking separately the expected spatial overlap among ticks and reservoirs for these pathogens in Europe. Environmental traits were obtained from MODIS satellite images for the years 2002-2017 (baseline) and projected on scenarios for the years 2030 and 2050. The ratio between MODIS baseline/current interpolated climatologies (WorldClim), and the ratio between MODIS-projected year 2050 with five climate change scenarios for that year (WorldClim) revealed no significant differences, meaning that projections from MODIS are reliable. Models predict that contact rates between the tick and reservoirs of either B. garinii or B. afzelii are spatially different because those have different habitats overlap. This is expected to promote different distribution patterns because of the different responses of both groups of reservoirs to environmental variables. Models for 2030 predict an increase in latitude, mainly in the circulation of B. garinii, with large areas of expected permanent contact between vector and reservoirs in Nordic countries and central Europe. However, climate projections for the year 2050 predict an unexpected scenario of contact disruption. Though large areas in Europe would be suitable for circulation of the pathogens, the predicted lack of niche overlap among ticks and reservoirs could promote a decrease in permanent foci. This development represents a proof-of-concept for the power of jointly modeling both the vector and reservoirs in a common framework. A deeper understanding of the unanticipated result regarding the year 2050 is needed.

A Retrospective Assessment of Temperature Trends in Northern Europe Reveals a Deep Impact on the Life Cycle of Ixodes ricinus (Acari: Ixodidae).

: This study modelled the changes in the development processes of the health-threatening tick Ixodes ricinus in Northern Europe as driven by the trends of temperature (1950-2018). We used the ECA&D dataset to calculate the annual accumulated temperature to obtain the development rates of the oviposition, incubation, larva-nymph, and nymph-adult molts. Annual values were used to ascertain the trend in development rates of each stage. The ecological classification of Northern Europe (LANMAP2) was used to summarize results. The temperature in 1950-2018 clearly increased in the target territory. The development rates of every tested life cycle process were faster along the time series. Faster oviposition and incubation rates resulted in central Sweden, Baltic countries, and parts of Finland. Faster molting rates were observed in the same territories and in large areas of Western Norway. The trend of temperature in the period 1950-2018 shows a consistent inflection point around 1990, demonstrating that the increased annual accumulated temperature has a deeper impact on the life cycle of I. ricinus since approximately 1990. Faster development rates could be part of the processes driving the reported spread of the tick in the target area and should be considered as a serious threat to human health.

Stray dogs in Nepal have high prevalence of vector-borne pathogens: a molecular survey.

BACKGROUND: Population of stray dogs is significant in large cities of Nepal, such as Kathmandu. Most of stray dogs suffer a lack of basic health care. Considering the clinical relevance, the broad distribution and the lack of information of canine vector borne diseases (CVBD) in Nepal, the aim of this study was to evaluate the prevalence of different vector-borne pathogens (VBP) in stray dogs living in the metropolitan area of Kathmandu, and to assess different traits as possible risk factors. METHODS: A total of 70 canine blood samples from stray dogs attended at the Kathmandu Animal Treatment Centre during August 2017 were collected on filter paper (Flinders Technology Associates (FTA) cards). Data regarding signalment, clinical signs and epidemiological characteristics were recorded for each animal. Real-time polymerase chain reaction assays were performed for Leishmania spp., Ehrlichia spp./Anaplasma spp., Babesia spp./Theileria spp. and Hepatozoon canis. RESULTS: The overall prevalence detected was 31.43% for Hepatozoon canis, 31.43% for Anaplasma platys, 27.14% for Ehrlichia canis, 18.57% for Leishmania donovani species complex, 12.86% for isolates corresponding to Theileria spp., 12.86% for Babesia vogeli and 2.86% for B. gibsoni. A total of 81.43% of the dogs were positive to at least one of the VBP tested. Co-infections were detected in 41.43% of the dogs. Dogs positive to any of the VBP tested, and particularly to E. canis, were older than those that were negative. CONCLUSIONS: To our knowledge, this is the first molecular detection of VBP in stray dogs from Kathmandu, Nepal. The high prevalence of VBP detected highlights the need to implement a surveillance programme and control strategies for these CVBD in the population of stray dogs in this area.