Sequences Related to Chimay Rhabdovirus Are Widely Distributed in Ixodes ricinus Ticks across England and Wales.

Ticks are the main arthropod vector of pathogens to humans and livestock in the British Isles. Despite their role as a vector of disease, many aspects of tick biology, ecology, and microbial association are poorly understood. To address this, we investigated the composition of the microbiome of adult and nymphal Ixodes ricinus ticks. The ticks were collected on a dairy farm in Southwest England and RNA extracted for whole genome sequencing. Sequences were detected from a range of microorganisms, particularly tick-associated viruses, bacteria, and nematodes. A majority of the viruses were attributed to phlebo-like and nairo-like virus groups, demonstrating a high degree of homology with the sequences present in I. ricinus from mainland Europe. A virus sharing a high sequence identity with Chimay rhabdovirus, previously identified in ticks from Belgium, was detected. Further investigations of I. ricinus ticks collected from additional sites in England and Wales also identified Chimay rhabdovirus viral RNA with varying prevalence in all tick populations. This suggests that Chimay rhabdovirus has a wide distribution and highlights the need for an extended exploration of the tick microbiome in the United Kingdom (UK).

Detection of Babesia species in questing Ixodes ricinus ticks in England and Wales.

Babesiosis, a disease in humans and animals is caused by piroplasms from the genus Babesia and is transmitted by ixodid ticks. Bovine babesiosis, commonly called redwater fever, is reported in cattle from many regions of the British Isles. The presence of Babesia in questing ticks in the United Kingdom (UK) and its potential impact on public and animal health has not been widely studied. Therefore, this study aimed to assess the presence of Babesia spp. in England and Wales using ticks collected over a six-year period. Questing Ixodes ricinus nymphs were collected at 20 recreational areas between 2014 and 2019 and screened for Babesia. Of 3912 nymphs tested, Babesia spp. were detected in 15, giving an overall prevalence of 0.38% [95%CI: 0.21-0.63%]. A number of Babesia species were identified including B. venatorum (n = 9), B. divergens/capreoli (n = 5) and B. odocoilei-like species (n = 1). Based on the low prevalence of Babesia detected in questing I. ricinus nymphs in the recreational areas studied, the likelihood of exposure to Babesia-infected ticks is lower compared to other pathogens more widely studied in the UK (e.g. Borrelia burgdorferi s.l.). However, localized areas of elevated risk may occur in pockets in England and Wales.

Anaplasma phagocytophilum Ecotype Analysis in Cattle from Great Britain.

Anaplasma phagocytophilum (A. phagocytophilum) is the aetiological agent of tick-borne fever in cattle and sheep, and granulocytic anaplasmosis in human and dogs. Livestock, companion animal and human infections with A. phagocytophilum have been reported globally. Across England and Wales, two isolates (called ecotypes) have been reported in ticks. This study examined A. phagocytophilum isolates present in livestock and wildlife in Great Britain (GB), with a particular focus on cattle. Clinical submissions (EDTA blood) from cattle (n = 21) and sheep (n = 3) were received by APHA for tick-borne disease testing and the animals were confirmed to be infected with A. phagocytophilum using a PCR targeting the Msp2 gene. Further submissions from roe deer (n = 2), red deer (n = 2) and Ixodes ricinus ticks (n = 22) were also shown to be infected with A. phagocytophilum. Subsequent analysis using a nested PCR targeting the groEL gene and sequencing confirmed the presence of ecotype I in cattle, sheep, red deer and Ixodes ricinus, and ecotype II in roe deer and I. ricinus removed from deer carcasses. Despite the presence of two ecotypes, widely distributed in ticks from England and Wales, only ecotype I was detected in cattle in this study.

Possible expansion of Ixodes ricinus in the United Kingdom identified through the Tick Surveillance Scheme between 2013 and 2020.

The tick Ixodes ricinus (Ixodida: Ixodidae, Linnaeus) is the main vector of several pathogens including Borrelia burgdorferi s.l. (agent of Lyme borreliosis) and tick-borne encephalitis virus. Its distribution depends on many factors including suitable habitat, climate and presence of hosts. In this study, we present records of I. ricinus bites on humans, dogs (Canis lupus familiaris; Carnivora: Canidae, L.) and cats (Felis catus; Carnivora: Felidiae, L.) in the United Kingdom (UK) obtained through the Tick Surveillance Scheme between 2013 and 2020. We divided the UK into 20 km x 20 km grids and 9.2% (range 1.2%-30%) of grids had at least one record every year since 2013. Most regions reported a yearly increase in the percentage of grids reporting I. ricinus since 2013 and the highest changes occurred in the South and East England with 5%-6.7% of new grids reporting I. ricinus bites each year in areas that never reported ticks before. Spatiotemporal analyses suggested that, while all regions recorded I. ricinus in new areas every year, there was a yearly decline in the percentage of new areas covered, except for Scotland. We discuss potential drivers of tick expansion, including reforestation and increase in deer populations.

Mapping and monitoring tick (Acari, Ixodida) distribution, seasonality, and host associations in the United Kingdom between 2017 and 2020.

Tick-borne disease risk is intrinsically linked to the distribution of tick vector species. To assess risk and anticipate disease emergence, an understanding of tick distribution, host associations, and seasonality is needed. This can be achieved, to some extent, using passive surveillance supported by engagement with the public, animal health, and public health experts. The Tick Surveillance Scheme (TSS) collects data and maps tick distribution across the United Kingdom (UK). Between 2017 and 2020, 3720 tick records were received and 39 tick species were detected. Most records were acquired in the UK, with a subset associated with recent overseas travel. The dominant UK acquired species was Ixodes ricinus (Ixodida: Ixodidae, Linnaeus), the main vector of Lyme borreliosis. Records peaked during May and June, highlighting a key risk period for tick bites. Other key UK species were detected, including Dermacentor reticulatus (Ixodida: Ixodidae, Fabricius) and Haemaphysalis punctata (Ixodida: Ixodidae, Canestrini & Fanzago) as well as several rarer species that may present novel tick-borne disease risk to humans and other animals. Updated tick distribution maps highlight areas in the UK where tick exposure has occurred. There is evidence of increasing human tick exposure over time, including during the COVID-19 pandemic, but seasonal patterns remain unchanged.

No net effect of host density on tick-borne disease hazard due to opposing roles of vector amplification and pathogen dilution.

To better understand vector-borne disease dynamics, knowledge of the ecological interactions between animal hosts, vectors, and pathogens is needed. The effects of hosts on disease hazard depends on their role in driving vector abundance and their ability to transmit pathogens. Theoretically, a host that cannot transmit a pathogen could dilute pathogen prevalence but increase disease hazard if it increases vector population size. In the case of Lyme disease, caused by Borrelia burgdorferi s.l. and vectored by Ixodid ticks, deer may have dual opposing effects on vectors and pathogen: deer drive tick population densities but do not transmit B. burgdorferi s.l. and could thus decrease or increase disease hazard. We aimed to test for the role of deer in shaping Lyme disease hazard by using a wide range of deer densities while taking transmission host abundance into account. We predicted that deer increase nymphal tick abundance while reducing pathogen prevalence. The resulting impact of deer on disease hazard will depend on the relative strengths of these opposing effects. We conducted a cross-sectional survey across 24 woodlands in Scotland between 2017 and 2019, estimating host (deer, rodents) abundance, questing Ixodes ricinus nymph density, and B. burgdorferi s.l. prevalence at each site. As predicted, deer density was positively associated with nymph density and negatively with nymphal infection prevalence. Overall, these two opposite effects canceled each other out: Lyme disease hazard did not vary with increasing deer density. This demonstrates that, across a wide range of deer and rodent densities, the role of deer in amplifying tick densities cancels their effect of reducing pathogen prevalence. We demonstrate how noncompetent host density has little effect on disease hazard even though they reduce pathogen prevalence, because of their role in increasing vector populations. These results have implications for informing disease mitigation strategies, especially through host management.

Spatial and temporal heterogeneity of the density of Borrelia burgdorferi-infected Ixodes ricinus ticks across a landscape: A 5-year study in southern England.

The density of Borrelia burgdorferi-infected Ixodes ricinus nymphs (DIN) was investigated during 2013-2017 across a Lyme disease-endemic landscape in southern England. The density of nymphs (DON), nymph infection prevalence (NIP), and DIN varied across five different natural habitats, with the highest DIN in woodland edge and high biodiversity woodlands. DIN was significantly lower in scrub grassland compared to the woodland edge, with low DON and no evidence of infection in ticks in non-scrub grassland. Over the 5 years, DON, NIP and DIN were comparable within habitats, except in 2014, with NIP varying three-fold and DIN significantly lower compared to 2015-2017. Borrelia garinii was most common, with bird-associated Borrelia (B. garinii/valaisiana) accounting for ~70% of all typed sequences. Borrelia burgdorferi sensu stricto was more common than B. afzelii. Borrelia afzelii was more common in scrub grassland than woodland and absent in some years. The possible impact of scrub on grazed grassland, management of ecotonal woodland margins with public access, and the possible role of birds/gamebirds impacting NIP are discussed. Mean NIP was 7.6%, highlighting the potential risk posed by B. burgdorferi in this endemic area. There is a need for continued research to understand its complex ecology and identify strategies for minimizing risk to public health, through habitat/game management and public awareness.

Prevalence of Anaplasma phagocytophilum in questing Ixodes ricinus nymphs across twenty recreational areas in England and Wales.

Human granulocytic anaplasmosis and tick-borne fever, affecting livestock, are diseases caused by an infection with the bacterium Anaplasma phagocytophilum. Its transmission dynamics between vertebrate hosts and ticks remain largely unknown and the potential impact on public health in the United Kingdom is unclear. This study aimed to assess the distribution and estimate the prevalence of A. phagocytophilum in questing Ixodes ricinus at recreational locations across England and Wales over six years. An additional objective was to investigate possible associations between prevalence, habitat and presence of ruminant hosts. Ixodes ricinus ticks were collected each spring at 20 recreational locations across England and Wales between 2014 and 2019. Nymphs were tested for infection with A. phagocytophilum by detection of bacterial genome in DNA extracts, targeting the msp2 gene locus. Positive samples were further investigated for the presence of different ecotypes based on the GroEL region. Of 3,919 nymphs tested, the mean infection prevalence was 3.6% [95%CI: 3.1-4.3] and ranged from 0 to 20.4%. Northern England had a higher overall prevalence (4.7% [95%CI: 3.4-6.4]) compared to Southern England (1.8% [95%CI: 1.3-2.5]) and the presence of sheep was associated with higher A. phagocytophilum prevalence (8.4% [95%CI: 6.9-10.1] vs 1.2% [95%CI: 0.8-1.7] when absent). There was also a negative correlation with the prevalence of Borrelia burgdorferi s.l. (causing Lyme borreliosis). When investigating the diversity of A. phagocytophilum, ecotype I accounted for 86.8% of samples and ecotype II for 13.2%. Our study presents an overview of A. phagocytophilum prevalence in questing I. ricinus in recreational areas across England and Wales and discusses the potential public and veterinary health relevance.

Experimental evidence for opposing effects of high deer density on tick-borne pathogen prevalence and hazard.

BACKGROUND: Identifying the mechanisms driving disease risk is challenging for multi-host pathogens, such as Borrelia burgdorferi sensu lato (s.l.), the tick-borne bacteria causing Lyme disease. Deer are tick reproduction hosts but do not transmit B. burgdorferi s.l., whereas rodents and birds are competent transmission hosts. Here, we use a long-term deer exclosure experiment to test three mechanisms for how high deer density might shape B. burgdorferi s.l. prevalence in ticks: increased prevalence due to higher larval tick densities facilitating high transmission on rodents (M1); alternatively, reduced B. burgdorferi s.l. prevalence because more larval ticks feed on deer rather than transmission-competent rodents (dilution effect) (M2), potentially due to ecological cascades, whereby higher deer grazing pressure shortens vegetation which decreases rodent abundance thus reducing transmission (M3). METHODS: In a large enclosure where red deer stags were kept at high density (35.5 deer km-2), we used an experimental design consisting of eight plots of 0.23 ha, four of which were fenced to simulate the absence of deer and four that were accessible to deer. In each plot we measured the density of questing nymphs and nymphal infection prevalence in spring, summer and autumn, and quantified vegetation height and density, and small mammal abundance. RESULTS: Prevalence tended to be lower, though not conclusively so, in high deer density plots compared to exclosures (predicted prevalence of 1.0% vs 2.2%), suggesting that the dilution and cascade mechanisms might outweigh the increased opportunities for transmission mechanism. Presence of deer at high density led to shorter vegetation and fewer rodents, consistent with an ecological cascade. However, Lyme disease hazard (density of infected I. ricinus nymphs) was five times higher in high deer density plots due to tick density being 18 times higher. CONCLUSIONS: High densities of tick reproduction hosts such as deer can drive up vector-borne disease hazard, despite the potential to simultaneously reduce pathogen prevalence. This has implications for environmental pathogen management and for deer management, although the impact of intermediate deer densities now needs testing.

Ixodes ricinus and Borrelia burgdorferi sensu lato in the Royal Parks of London, UK.

Assessing the risk of tick-borne disease in areas with high visitor numbers is important from a public health perspective. Evidence suggests that tick presence, density, infection prevalence and the density of infected ticks can vary between habitats within urban green space, suggesting that the risk of Lyme borreliosis transmission can also vary. This study assessed nymph density, Borrelia prevalence and the density of infected nymphs across a range of habitat types in nine parks in London which receive millions of visitors each year. Ixodes ricinus were found in only two of the nine locations sampled, and here they were found in all types of habitat surveyed. Established I. ricinus populations were identified in the two largest parks, both of which had resident free-roaming deer populations. Highest densities of nymphs (15.68 per 100 m2) and infected nymphs (1.22 per 100 m2) were associated with woodland and under canopy habitats in Richmond Park, but ticks infected with Borrelia were found across all habitat types surveyed. Nymphs infected with Borrelia (7.9%) were only reported from Richmond Park, where Borrelia burgdorferi sensu stricto and Borrelia afzelii were identified as the dominant genospecies. Areas with short grass appeared to be less suitable for ticks and maintaining short grass in high footfall areas could be a good strategy for reducing the risk of Lyme borreliosis transmission to humans in such settings. In areas where this would create conflict with existing practices which aim to improve and/or meet historic landscape, biodiversity and public access goals, promoting public health awareness of tick-borne disease risks could also be utilised.