Investigation of a Human Case of Francisella tularensis Infection, United Kingdom, 2023.

Tularemia, caused by Francisella tularensis, is not known to occur in the United Kingdom. We report a case of tularemia diagnosed in July 2023 in a UK patient with no travel in the 6 weeks before symptom onset. We describe the subsequent multiagency investigation into possible routes of acquisition.

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.

VectorNet: collaborative mapping of arthropod disease vectors in Europe and surrounding areas since 2010.

BackgroundArthropod vectors such as ticks, mosquitoes, sandflies and biting midges are of public and veterinary health significance because of the pathogens they can transmit. Understanding their distributions is a key means of assessing risk. VectorNet maps their distribution in the EU and surrounding areas.AimWe aim to describe the methodology underlying VectorNet maps, encourage standardisation and evaluate output.Methods: Vector distribution and surveillance activity data have been collected since 2010 from a combination of literature searches, field-survey data by entomologist volunteers via a network facilitated for each participating country and expert validation. Data were collated by VectorNet members and extensively validated during data entry and mapping processes.ResultsAs of 2021, the VectorNet archive consisted of ca 475,000 records relating to > 330 species. Maps for 42 species are routinely produced online at subnational administrative unit resolution. On VectorNet maps, there are relatively few areas where surveillance has been recorded but there are no distribution data. Comparison with other continental databases, namely the Global Biodiversity Information Facility and VectorBase show that VectorNet has 5-10 times as many records overall, although three species are better represented in the other databases. In addition, VectorNet maps show where species are absent. VectorNet's impact as assessed by citations (ca 60 per year) and web statistics (58,000 views) is substantial and its maps are widely used as reference material by professionals and the public.ConclusionVectorNet maps are the pre-eminent source of rigorously validated arthropod vector maps for Europe and its surrounding areas.

The Genetic Diversity of Rickettsiella Symbionts in Ixodes ricinus Throughout Europe.

Rickettsiella species are bacterial symbionts that are present in a great variety of arthropod species, including ixodid ticks. However, little is known about their genetic diversity and distribution in Ixodes ricinus, as well as their relationship with other tick-associated bacteria. In this study, we investigated the occurrence and the genetic diversity of Rickettsiella spp. in I. ricinus throughout Europe and evaluated any preferential and antagonistic associations with Candidatus Midichloria mitochondrii and the pathogens Borrelia burgdorferi sensu lato and Borrelia miyamotoi. Rickettsiella spp. were detected in most I. ricinus populations investigated, encompassing a wide array of climate types and environments. The infection prevalence significantly differed between geographic locations and was significantly higher in adults than in immature life stages. Phylogenetic investigations and protein characterization disclosed four Rickettsiella clades (I-IV). Close phylogenetic relations were observed between Rickettsiella strains of I. ricinus and other arthropod species. Isolation patterns were detected for Clades II and IV, which were restricted to specific geographic areas. Lastly, although coinfections occurred, we did not detect significant associations between Rickettsiella spp. and the other tick-associated bacteria investigated. Our results suggest that Rickettsiella spp. are a genetically and biologically diverse facultative symbiont of I. ricinus and that their distribution among tick populations could be influenced by environmental components.

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.

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.

Tick-Borne Encephalitis Virus, United Kingdom.

During February 2018-January 2019, we conducted large-scale surveillance for the presence and prevalence of tick-borne encephalitis virus (TBEV) and louping ill virus (LIV) in sentinel animals and ticks in the United Kingdom. Serum was collected from 1,309 deer culled across England and Scotland. Overall, 4% of samples were ELISA-positive for the TBEV serocomplex. A focus in the Thetford Forest area had the highest proportion (47.7%) of seropositive samples. Ticks collected from culled deer within seropositive regions were tested for viral RNA; 5 of 2,041 ticks tested positive by LIV/TBEV real-time reverse transcription PCR, all from within the Thetford Forest area. From 1 tick, we identified a full-length genomic sequence of TBEV. Thus, using deer as sentinels revealed a potential TBEV focus in the United Kingdom. This detection of TBEV genomic sequence in UK ticks has important public health implications, especially for undiagnosed encephalitis.

Potential for Zika virus transmission by mosquitoes in temperate climates.

Mosquito-borne Zika virus (ZIKV) transmission has almost exclusively been detected in the tropics despite the distributions of its primary vectors extending farther into temperate regions. Therefore, it is unknown whether ZIKV's range has reached a temperature-dependent limit, or if it can spread into temperate climates. Using field-collected mosquitoes for biological relevance, we found that two common temperate mosquito species, Aedes albopictus and Ochlerotatus detritus, were competent for ZIKV. We orally exposed mosquitoes to ZIKV and held them at between 17 and 31°C, estimated the time required for mosquitoes to become infectious, and applied these data to a ZIKV spatial risk model. We identified a minimum temperature threshold for the transmission of ZIKV by mosquitoes between 17 and 19°C. Using these data, we generated standardized basic reproduction number R0-based risk maps and we derived estimates for the length of the transmission season for recent and future climate conditions. Our standardized R0-based risk maps show potential risk of ZIKV transmission beyond the current observed range in southern USA, southern China and southern European countries. Transmission risk is simulated to increase over southern and Eastern Europe, northern USA and temperate regions of Asia (northern China, southern Japan) in future climate scenarios.

A probable case of tick-borne encephalitis (TBE) acquired in England, July 2019.

The United Kingdom (UK) has thus far been considered to be free from tick-borne encephalitis (TBE), yet in July 2019, a German infant developed serologically diagnosed TBE following a tick bite in southern England. This first report of a probable human case together with recent findings of TBE virus in ticks in foci in England suggest that TBE may be acquired in parts of England and should be considered in patients with aetiologically-unexplained neurological manifestations.

Detection of new endemic focus of tick-borne encephalitis virus (TBEV), Hampshire/Dorset border, England, September 2019.

The presence of tick-borne encephalitis virus (TBEV) was detected in a questing tick pool in southern England in September 2019. Hitherto, TBEV had only been detected in a limited area in eastern England. This southern English viral genome sequence is distinct from TBEV-UK, being most similar to TBEV-NL. The new location of TBEV presence highlights that the diagnosis of tick-borne encephalitis should be considered in encephalitic patients in areas of the United Kingdom outside eastern England.

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).

Modelling the temperature dependent extrinsic incubation period of West Nile Virus using Bayesian time delay models.

West Nile Virus (WNV) is a mosquito-borne pathogen that primarily infects birds. Infections can spillover to humans and cause a spectrum of clinical symptoms, including WNV neuroinvasive disease. The extrinsic incubation period (EIP) is the time taken for a mosquito to become infectious following the ingestion of an infected blood meal. Characterising how the EIP varies with temperature is an essential part of predicting the impact and transmission dynamics of WNV. We re-analyse existing experimental data using Bayesian time delay models, allowing us to account for variation in how quickly individual mosquitoes developed disseminated WNV infections. In these experiments, cohorts of Culex pipiens mosquitoes were infected with WNV and kept under different temperature conditions, being checked for disseminated infection at defined timepoints. We find that EIPs are best described with a Weibull distribution and become shorter log-linearly with temperature. Under 18°C, less than 1% of infected Cx. pipiens had a disseminated infection after 5 days, compared to 9.73% (95% CrI: 7.97 to 11.54) at 25°C and 42.20% (95% CrI: 38.32 to 46.60) at 30°C. In the hottest experimental temperature treatment (32°C), the EIP50 was estimated at 3.78 days (CrI: 3.42 to 4.15) compared to over 100 days in the coolest treatment (15°C). The variance of EIPs was found to be much larger at lower temperatures than higher temperatures, highlighting the importance of characterising the time delay distribution associated with the EIP. We additionally demonstrate a competitive advantage of WNV strain WN02 over NY99, where the former infects mosquitoes more quickly at colder temperatures than the latter. This research contributes crucial parameters to the WNV literature, providing essential insights for modellers and those planning interventions.

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.

Risk factors for tick attachment in companion animals in Great Britain: a spatiotemporal analysis covering 2014-2021.

BACKGROUND: Ticks are an important driver of veterinary health care, causing irritation and sometimes infection to their hosts. We explored epidemiological and geo-referenced data from > 7 million electronic health records (EHRs) from cats and dogs collected by the Small Animal Veterinary Surveillance Network (SAVSNET) in Great Britain (GB) between 2014 and 2021 to assess the factors affecting tick attachment in an individual and at a spatiotemporal level. METHODS: EHRs in which ticks were mentioned were identified by text mining; domain experts confirmed those with ticks on the animal. Tick presence/absence records were overlaid with a spatiotemporal series of climate, environment, anthropogenic and host distribution factors to produce a spatiotemporal regression matrix. An ensemble machine learning spatiotemporal model was used to fine-tune hyperparameters for Random Forest, Gradient-boosted Trees and Generalized Linear Model regression algorithms, which were then used to produce a final ensemble meta-learner to predict the probability of tick attachment across GB at a monthly interval and averaged long-term through 2014-2021 at a spatial resolution of 1 km. Individual host factors associated with tick attachment were also assessed by conditional logistic regression on a matched case-control dataset. RESULTS: In total, 11,741 consultations were identified in which a tick was recorded. The frequency of tick records was low (0.16% EHRs), suggesting an underestimation of risk. That said, increased odds for tick attachment in cats and dogs were associated with younger adult ages, longer coat length, crossbreeds and unclassified breeds. In cats, males and entire animals had significantly increased odds of recorded tick attachment. The key variables controlling the spatiotemporal risk for tick attachment were climatic (precipitation and temperature) and vegetation type (Enhanced Vegetation Index). Suitable areas for tick attachment were predicted across GB, especially in forests and grassland areas, mainly during summer, particularly in June. CONCLUSIONS: Our results can inform targeted health messages to owners and veterinary practitioners, identifying those animals, seasons and areas of higher risk for tick attachment and allowing for more tailored prophylaxis to reduce tick burden, inappropriate parasiticide treatment and potentially TBDs in companion animals and humans. Sentinel networks like SAVSNET represent a novel complementary data source to improve our understanding of tick attachment risk for companion animals and as a proxy of risk to humans.

UK mosquitoes are competent to transmit Usutu virus at native temperatures.

Usutu virus (USUV) is an emerging zoonotic virus transmitted primarily by Culex mosquitoes. Since its introduction into Europe from Africa during the late 20th century, it has caused mortality within populations of passerine birds and captive owls, and can on occasion lead to disease in humans. USUV was first detected in the UK in 2020 and has become endemic, having been detected in either birds and/or mosquitoes every subsequent year. Importantly, the vector competence of indigenous mosquitoes for the circulating UK (London) USUV strain at representative regional temperatures is still to be elucidated. This study assessed the vector competence of five field-collected mosquito species/biotypes, Culex pipiens biotype molestus, Culex pipiens biotype pipiens, Culex torrentium, Culiseta annulata and Aedes detritus for the London USUV strain, with infection rates (IR) and transmission rates (TR) evaluated between 7 and 28 days post-infection. Infection and transmission were observed in all species/biotypes aside from Ae. detritus and Cx. torrentium. For Cx. pipiens biotype molestus, transmission potential suggests these populations should be monitored further for their role in transmission to humans. Furthermore, both Cx. pipiens biotype pipiens and Cs. annulata were shown to be competent vectors at 19 °C indicating the potential for geographical spread of the virus to other UK regions.

Field-based assessments of the seasonality of Culex pipiens sensu lato in England: an important enzootic vector of Usutu and West Nile viruses.

BACKGROUND: Usutu virus (USUV), which is closely related to West Nile virus (WNV), sharing a similar ecology and transmission cycle, was first reported in the UK in the southeast of England in 2020. Both USUV and WNV are emerging zoonotic viruses hosted by wild birds. The 2020 finding of USUV in England raised awareness of this virus and highlighted the importance of understanding the seasonality of Culex pipiens sensu lato (Cx. pipiens s.l.), the main enzootic vector of these viruses. Zoos are prime locations for trapping mosquitoes because of their infrastructure, security, and range of vertebrate hosts and aquatic habitats. METHODS: Three independent zoo-based case studies at four locations that cover the seasonality of Cx. pipiens s.l. in England were undertaken: (i) London Zoo (Zoological Society London [ZSL]) and surrounding areas, London; (ii) Chester Zoo (Cheshire); (ii) Twycross Zoo (Leicestershire); and (iv) Flamingo Land (zoo; North Yorkshire). Various adult mosquito traps were used to catch adult Cx. pipiens s.l. across seasons. RESULTS: High yields of Cx. pipiens s.l./Culex torrentium were observed in Biogents-Mosquitaire and Center for Disease Control and Prevention Gravid traps in all studies where these traps were used. Mosquito counts varied between sites and between years. Observations of adult Cx. pipiens s.l./Cx. torrentium abundance and modelling studies demonstrated peak adult abundance between late July and early August, with active adult female Cx. pipiens s.l./Cx. torrentium populations between May and September. CONCLUSIONS: The information collated in this study illustrates the value of multiple mosquito monitoring approaches in zoos to describe the seasonality of this UK vector across multiple sites in England and provides a framework that can be used for ongoing and future surveillance programmes and disease risk management strategies.

Challenges in undertaking mosquito surveillance at UK seaports and airports to prevent the entry and establishment of invasive vector species.

Port health authorities have played an important role in the control of infectious diseases worldwide. The International Health Regulations (2005) further clarifies this role and provides a legal statutory instrument that aims to assist the international community to prevent and respond to global public health risks. Eleven UK sea and airports participated in a pilot, investigating the challenges ports could face in attempting to monitor for mosquitoes. The study also examined the types of habitat that could support mosquitoes. There is a concern that exotic vector species, such as Aedes albopictus, could invade and become established in the UK. Environments in and around the ports differed, and this was reflected in the species of mosquitoes caught. Ports used different methods to collect mosquitoes and developed a range of techniques for surveying, which suited the conditions at their port. This paper discusses the implications of invasive mosquito surveillance to UK port health authorities.

Modelling the current and future temperature suitability of the UK for the vector Hyalomma marginatum (Acari: Ixodidae).

Hyalomma marginatum is the main vector of Crimean-Congo haemorrhagic fever virus (CCHFV) and spotted fever rickettsiae in Europe. The distribution of H. marginatum is currently restricted to parts of southern Europe, northern Africa and Asia, and one of the drivers limiting distribution is climate, particularly temperature. As temperatures rise with climate change, parts of northern Europe currently considered too cold for H. marginatum to be able to survive may become suitable, including the United Kingdom (UK), presenting a potential public health concern. Here we use a series of modelling methodologies to understand whether mean air temperatures across the UK during 2000-2019 were sufficient for H. marginatum nymphs to moult into adult stages and be able to overwinter in the UK if they were introduced on migratory birds. We then used UK-specific climate projections (UKCP18) to determine whether predicted temperatures would be sufficient to allow survival in future. We found that spring temperatures in parts of the UK during 2000-2019 were warm enough for predicted moulting to occur, but in all years except 2006, temperatures during September to December were too cold for overwintering to occur. Our analysis of the projections data suggests that whilst temperatures in the UK during September to December will increase in future, they are likely to remain below the threshold required for H. marginatum populations to become established.

Ixodes ricinus density, Borrelia prevalence and the density of infected nymphs along an urban-rural gradient in southern England.

Ticks are found across a range of habitats, with woodland being particularly important for high densities and prevalence of Borrelia infection. Assessments of risk in urban woodland can be difficult if there are low densities and small sample sizes for Borrelia prevalence estimates. This study targeted six urban woodlands with established tick populations, as well as six woodlands in peri-urban zones and six woodlands in rural zones in and around the cities of Bath and Southampton, in the South of England. Nymph densities were estimated, and 100 nymphs were tested from each of the 18 woodlands studied. Ixodes ricinus ticks were found in all woodlands surveyed, and overall density of nymphs (DON) per 100 m2 was 18.17 in urban woodlands, 26.0 in peri-urban woodlands and 17.67 in rural woodlands. Out of 600 nymphs tested across urban woodlands, 10.3% were infected with Borrelia. The same proportion of nymphs collected in rural woodlands were positive for Borrelia. In peri-urban woodlands, 10.8% of nymphs tested positive. Across both cities combined, density of infected nymphs (DIN) was 2.73 per 100 m2 in peri-urban woodland, 1.87 per 100 m2 in urban woodland and 1.82 per 100 m2 in rural woodland. Overall, DON, Borrelia prevalence and DIN did not differ significantly along an urban-rural gradient. This suggests the risk of Lyme borreliosis transmission could be similar, or perhaps even elevated in urban woodland if there is higher public footfall, subsequent contact with ticks and less awareness of the risks. This is particularly important from a public health perspective, as Borrelia garinii dominated across the gradient and this genospecies is linked to neuroborreliosis.