Surveillance and Risk Analysis for Bovine Babesiosis in England and Wales to Inform Disease Distribution.

Babesia divergens is a zoonotic piroplasm that infects both cattle and humans in Europe. Disease transmission occurs through Ixodes ricinus tick bites, a species that is increasing in abundance and distribution across Europe in response to climate and land-use changes. Developments in agri-environment policy and changing consumer demands may also have unintended consequences on tick-borne disease rates. Currently, B. divergens surveillance in British cattle is limited, rendering temporal trend analysis and the detection of potential zoonotic hotspots impossible. The objective of this study was to assess syndromic surveillance as a means of determining babesiosis distribution in British cattle, and to evaluate the intrinsic disease risk factors in order to respond to disease threats posed by changing environments. Samples from 95 clinically affected cattle on 70 unique holdings were screened for Babesia spp., using established blood smear examination techniques and a B. divergens-specific PCR method, between April and December 2021. B. divergens was detected in 45/95 animals (47.4%), with PCR offering the advantage of identification at species level. Infection with Anaplasma phagocytophilum was detected in 19/95 animals (20%). Co-infection was detected in five animals. The cases were recorded across multiple geographic regions and throughout the sampling period. Univariate logistic regression analysis failed to identify any statistically significant risk factors for B. divergens presence. This study demonstrates that bovine babesiosis is geographically widespread throughout England and Wales, placing a large proportion of the cattle population at risk of infection, with the potential for zoonotic transmission to humans.

Tick-borne encephalitis virus.

Tick-borne encephalitis (TBE) is caused by a neurotropic flavivirus, transmitted by the bite of Ixodes species tick vectors, and is increasing in incidence and expanding its geographical range throughout Eurasia and the Far East. Most infections are asymptomatic. However, between 2 and 30 % of cases may develop into severe neurological disease, long-term neurological sequelae or death. Diagnosis is based upon clinical signs of neurological disease and demonstration of virus-specific IgM and IgG antibodies. There is no specific antiviral treatment and supportive care is required for the various manifestations of disease. Vaccination is an effective way of preventing disease.

Detection of Borrelia and Babesia species in Haemaphysalis punctata ticks sampled in Southern England.

The distribution and population size of the red sheep tick (Haemaphysalis punctata) are increasing in Northern Europe, and in the United Kingdom reports of human biting by this species have increased in recent years. To assess the risk of tick-borne disease (TBD) transmission to humans and livestock by H. punctata, ticks sampled from sites in Southern England were screened using PCR for either Borrelia species or piroplasms over a three year period, 2018-2020. A total of 302 H. punctata were collected from eight locations. From these, two Babesia species associated with TBD infections in livestock, Babesia major and Babesia motasi, and the human pathogen Borrelia miyamotoi were detected, predominantly from a single location in Sussex. Consequently, the range expansion of this tick across Southern England may impact public and livestock health.

First report of human exposure to Hyalomma marginatum in England: Further evidence of a Hyalomma moulting event in north-western Europe?

Hyalomma marginatum is widely distributed across the Mediterranean, Northern Africa and the Middle East. Current climate conditions in Northern Europe are thought to limit the species' ability to moult to the adult stage. It is a vector of several pathogens of human and veterinary concern, including Crimean-Congo haemorrhagic fever virus, for which it is the primary vector in Europe. Here, we report the first human exposure to a locally acquired adult H. marginatum in England, and the second detection in England of Rickettsia aeschlimannii associated with imported Hyalomma.

The Unexpected Holiday Souvenir: The Public Health Risk to UK Travellers from Ticks Acquired Overseas.

Overseas travel to regions where ticks are found can increase travellers' exposure to ticks and pathogens that may be unfamiliar to medical professionals in their home countries. Previous studies have detailed non-native tick species removed from recently returned travellers, occasionally leading to travel-associated human cases of exotic tick-borne disease. There are 20 species of tick endemic to the UK, yet UK travellers can be exposed to many other non-native species whilst overseas. Here, we report ticks received by Public Health England's Tick Surveillance Scheme from humans with recent travel history between January 2006 and December 2018. Altogether, 16 tick species were received from people who had recently travelled overseas. Confirmed imports (acquired outside of the UK) were received from people who recently travelled to 22 countries. Possible imports (acquired abroad or within the UK) were received from people who had recently travelled to eight European countries. Species-specific literature reviews highlighted nine of the sixteen tick species are known to vector at least one tick-borne pathogen to humans in the country of acquisition, suggesting travellers exposed to ticks may be at risk of being bitten by a species that is a known vector, with implications for novel tick-borne disease transmission to travellers.

Detection of Usutu virus infection in wild birds in the United Kingdom, 2020.

In August 2020, as part of a long-term disease surveillance programme, Usutu virus was detected in five Eurasian blackbirds (Turdus merula) and one house sparrow (Passer domesticus) from Greater London, England. This was initially detected by reverse transcription-PCR and was confirmed by virus isolation and by immunohistochemical detection of flavivirus in tissues. Phylogenetic analysis identified Usutu virus African 3.2 lineage, which is prevalent in the Netherlands and Belgium, suggesting a potential incursion from mainland Europe.

An outbreak of bovine babesiosis in February, 2019, triggered by above average winter temperatures in southern England and co-infection with Babesia divergens and Anaplasma phagocytophilum.

BACKGROUND: Bovine babesiosis, commonly known as redwater fever, is a sporadic tick-borne disease in the United Kingdom. Outbreaks occur during the spring, summer and autumn months when ticks are active. This study reports the findings of an investigation of an outbreak of bovine babesiosis during the winter month of February, 2019. METHODS: DNA from blood, organ and tick samples taken from affected cattle were tested for the presence of piroplasm and Anaplasma phagocytophilum DNA using PCRs directed to the 18S rRNA gene and msp2 gene respectively. The species of piroplasm was confirmed by sequencing. RESULTS: Babesia divergens DNA was detected in the blood of five cattle displaying clinical signs of babesiosis within a herd of twenty. This parasite was also detected in three of ten ticks removed from one of the affected cattle. In addition, A. phagocytophilum was detected in three cattle tested and two of ten of the ticks. CONCLUSIONS: An outbreak of bovine babesiosis during February is unusual as the tick vector, Ixodes ricinus, does not generally become active until temperatures rise later in the year. February of 2019 was unusual as average temperatures during the first week of the month reached over 10 °C, well above historical averages that are typically below 5 °C, and a temperature at which ticks can become active. This unusual weather event is likely to have triggered tick questing, that combined with a co-infection with two tick-borne pathogens caused the severe outbreak of disease.

Emerging Threats to Animals in the United Kingdom by Arthropod-Borne Diseases.

Worldwide, arthropod-borne disease transmission represents one of the greatest threats to public and animal health. For the British Isles, an island group on the north-western coast of continental Europe consisting of the United Kingdom (UK) and the Republic of Ireland, physical separation offers a barrier to the introduction of many of the pathogens that affect animals on the rest of the continent. Added to this are strict biosecurity rules at ports of entry and the depauperate vector biodiversity found on the islands. Nevertheless, there are some indigenous arthropod-borne pathogens that cause sporadic outbreaks, such as the tick-borne louping ill virus, found almost exclusively in the British Isles, and a range of piroplasmid infections that are poorly characterized. These provide an ongoing source of infection whose emergence can be unpredictable. In addition, the risk remains for future introductions of both exotic vectors and the pathogens they harbor, and can transmit. Current factors that are driving the increases of both disease transmission and the risk of emergence include marked changes to the climate in the British Isles that have increased summer and winter temperatures, and extended the period over which arthropods are active. There have also been dramatic increases in the distribution of mosquito-borne diseases, such as West Nile and Usutu viruses in mainland Europe that are making the introduction of these pathogens through bird migration increasingly feasible. In addition, the establishment of midge-borne bluetongue virus in the near continent has increased the risk of wind-borne introduction of infected midges and the inadvertent importation of infected cattle. Arguably the greatest risk is associated with the continual increase in the movement of people, pets and trade into the UK. This, in particular, is driving the introduction of invasive arthropod species that either bring disease-causing pathogens, or are known competent vectors, that increase the risk of disease transmission if introduced. The following review documents the current pathogen threats to animals transmitted by mosquitoes, ticks and midges. This includes both indigenous and exotic pathogens to the UK. In the case of exotic pathogens, the pathway and risk of introduction are also discussed.

Hyalomma rufipes on an untraveled horse: Is this the first evidence of Hyalomma nymphs successfully moulting in the United Kingdom?

During September 2018, a tick was submitted to Public Health England's Tick Surveillance Scheme for identification. The tick was sent from a veterinarian who removed it from a horse in Dorset, England, with no history of overseas travel. The tick was identified as a male Hyalomma rufipes using morphological and molecular methods and then tested for a range of tick-borne pathogens including; Alkhurma virus, Anaplasma, Babesia, Bhanja virus, Crimean-Congo Haemorrhagic fever virus, Rickettsia and Theileria. The tick tested positive for Rickettsia aeschlimannii, a spotted fever group rickettsia linked to a number of human cases in Africa and Europe. This is the first time H. rufipes has been reported in the United Kingdom (UK), and the lack of travel by the horse (or any in-contact horses) suggests that this could also be the first evidence of successful moulting of a Hyalomma nymph in the UK. It is postulated that the tick was imported into the UK on a migratory bird as an engorged nymph which was able to complete its moult to the adult stage and find a host. This highlights that passive tick surveillance remains an important method for the detection of unusual species that may present a threat to public health in the UK. Horses are important hosts of Hyalomma sp. adults in their native range, therefore, further surveillance studies should be conducted to check horses for ticks in the months following spring bird migration; when imported nymphs may have had time to drop off their avian host and moult to adults. The potential human and animal health risks of such events occurring more regularly are discussed.

Has the red sheep tick, Haemaphysalis punctata, recently expanded its range in England?

The red sheep tick, Haemaphysalis punctata (Ixodida: Ixodidae), has been reported as present in the U.K. for more than a century; however, very little has been written about its distribution. In recent years, numbers of detections of this tick species reported to the Public Health England (PHE) Tick Surveillance Scheme have increased. This rise in the number of records may be attributable to increased tick surveillance activities or to the increased distribution of this species of tick in parts of England. This paper reviews published reports of H. punctata and all data held by the Biological Records Centre and PHE, and summarizes a number of field studies conducted by PHE and the Animal and Plant Health Agency over the past 8 years. It would appear from the evidence presented here that H. punctata may be expanding its range across the eastern part of the South Downs National Park, where there have also been reports of this tick species biting humans. It is possible that the movement of sheep between grassland sites is facilitating this spread. Further studies that better elucidate the ecology of this tick and its possible role as a vector of human and veterinary diseases are now warranted.

Detection of tick-borne bacteria and babesia with zoonotic potential in Argas (Carios) vespertilionis (Latreille, 1802) ticks from British bats.

Ticks host a wide range of zoonotic pathogens and are a significant source of diseases that affect humans and livestock. However, little is known about the pathogens associated with bat ticks. We have collected ectoparasites from bat carcasses over a seven year period. Nucleic acids (DNA and RNA) were extracted from 296 ticks removed from bats and the species designation was confirmed in all ticks as Argas (Carios) vespertilionis. A subset of these samples (n = 120) were tested for the presence of zoonotic pathogens by molecular methods. Babesia species, Rickettsia spp., within the spotted fever group (SFG), and Ehrlichia spp. were detected in ticks removed from 26 bats submitted from 14 counties across England. The prevalence of Rickettsia spp. was found to be highest in Pipistrellus pipistrellus from southern England. This study suggests that the tick species that host B. venatorum may include the genus Argas in addition to the genus Ixodes. As A. vespertilionis has been reported to feed on humans, detection of B. venatorum and SFG Rickettsia spp. could present a risk of disease transmission in England. No evidence for the presence of flaviviruses or Issyk-Kul virus (nairovirus) was found in these tick samples.

Emerging Tick-Borne Viruses in the Twenty-First Century.

Ticks, as a group, are second only to mosquitoes as vectors of pathogens to humans and are the primary vector for pathogens of livestock, companion animals, and wildlife. The role of ticks in the transmission of viruses has been known for over 100 years and yet new pathogenic viruses are still being detected and known viruses are continually spreading to new geographic locations. Partly as a result of their novelty, tick-virus interactions are at an early stage in understanding. For some viruses, even the principal tick-vector is not known. It is likely that tick-borne viruses will continue to emerge and challenge public and veterinary health long into the twenty-first century. However, studies focusing on tick saliva, a critical component of tick feeding, virus transmission, and a target for control of ticks and tick-borne diseases, point toward solutions to emerging viruses. The aim of this review is to describe some currently emerging tick-borne diseases, their causative viruses, and to discuss research on virus-tick interactions. Through focus on this area, future protein targets for intervention and vaccine development may be identified.

Emergence of Babesia canis in southern England.

BACKGROUND: The United Kingdom is considered free of autochthonous transmission of canine babesiosis although cases are reported in dogs associated with recent travel abroad. During the winter months of 2015/16, a cluster of cases of disease in dogs with signs suggestive of canine babesiosis were reported in Harlow, Essex. METHODS: Babesia species were detected in dog blood samples by Giemsa staining of blood smears and by pan-piroplasm PCRs. Babesia species were also detected in extracts of tick DNA using pan-piroplasm PCRs. DNA sequencing and phylogenetic analysis was used to confirm the species of Babesia present in dog blood and tick samples. Tick species were identified by PCR-sequencing based on amplification of the cytochrome c oxidase subunit one (cox1) gene. Dermacentor reticulatus ticks were sampled from field sites in England and Wales. RESULTS: Blood smear analysis on samples taken from some of the affected dogs confirmed the presence of a large Babesia species within erythrocytes. A tick recovered from one of these cases was identified as Dermacentor reticulatus, a species with a limited distribution in England and Wales, but a known vector of canine babesiosis in continental Europe. Babesia canis was subsequently identified in blood samples obtained from three clinical cases (all dogs) within the area and from ticks associated with these dogs. A field survey detected 17 adult D. reticulatus ticks from one area visited by the affected dogs. Fourteen of these ticks were shown to be positive for the B. canis parasite, implicating them as a potential source for babesiosis in Harlow. In order to assess whether the parasite is present in more than one tick population, D. reticulatus ticks from across England and Wales were screened for the presence of Babesia species. In addition to the Harlow site, a further five locations where D. reticulatus is present were screened for Babesia species. Babesia was not detected from most sites tested but one tick from a single location in Wales was positive for B. canis. CONCLUSIONS: Infection with B. canis was confirmed in a number of dogs in Harlow, Essex, with no history of travel outside of the country. The same pathogen was identified in field-caught D. reticulatus ticks in the same area and is considered the likely source of infection. This highlights the need for vigilance by veterinary surgeons for future outbreaks of tick-borne disease in dogs.

Distribution of the tick Dermacentor reticulatus in the United Kingdom.

The recent implication of Dermacentor reticulatus (Ixodida: Ixodidae) in the transmission of canine babesiosis in the U.K. has highlighted the lack of accurate published data on its distribution in this country. This paper aims to collate and appraise historical data for D. reticulatus, to supplement such data with more recent surveillance data and to report on field sampling conducted during 2009-2016. These updated data facilitate better understanding of the current distribution of this tick in the U.K., which will better inform disease risk assessments. There appear to be four known regions of the U.K. in which D. reticulatus currently occurs, including western Wales, North and South Devon, and Essex. The majority of foci are located in coastal sand dunes and maritime grasslands, including grazing marsh. However, more recently the tick has been detected in urban greenspace in Essex. The emergence of this tick as a vector of babesiosis in the U.K. and its recent apparent spread in Essex into urban greenspace highlight the need for continued surveillance and for further research into its status as a vector of human and veterinary pathogens.

Rhipicephalus sanguineus importation into the UK: surveillance, risk, public health awareness and One Health response.

As part of Public Health England's assessment of vectorborne disease risk to public health in the UK, tick specimens are regularly submitted by veterinarians for identification via the Tick Surveillance Scheme. Recently, a number of these specimens have been identified as the brown dog tick, Rhipicephalus sanguineus This species is non-endemic to the UK and presents a risk to both human and animal health due to its role in the transmission of various tickborne pathogens. Although current climatic conditions in the UK are unlikely to permit the survival of this species outdoors, indoor infestations can occur and this can present a risk of disease transmission within an infested property. This paper documents 40 importation events involving R sanguineus on recently travelled or imported dogs into the UK since 2012. It also provides details of the response following these detections in line with the One Health concept. With the increasing number of dogs travelling or being imported, it is likely that importation and infestation events in the UK will continue and may result in pathogen transmission. It is therefore important to raise awareness of this risk and share lessons learned to improve our prevention and response strategies to this emerging issue.

Detection of Theileria orientalis in mosquito blood meals in the United Kingdom.

Theileria spp. are tick-borne protozoan parasites that infect a wide range of wild and domestic animals. In this study, the utility of xenosurveillance of blood-fed specimens of Culiseta annulata for detecting the presence of piroplasms in livestock was investigated. Blood-fed mosquitoes were collected at Elmley National Nature Reserve, Kent, United Kingdom. All specimens were morphologically identified, and DNA barcoding was used to confirm the morphological identification. Both the vertebrate host species and Theileria genome was detected within the bloodmeal by real-time PCR. Sequencing was used to confirm the identity of all amplicons. In total, 105 blood-fed mosquitoes morphologically identified as Cs. annulata were collected. DNA barcoding revealed that 102 specimens were Cs. annulata (99%), while a single specimen was identified as Anopheles messeae. Two specimens could not be identified molecularly due to PCR amplification failure. Blood meal analysis revealed that Cs. annulata fed almost exclusively on cattle at the collection site (n=100). The application of a pan-piroplasm PCR detected 16 positive samples (15.2%) and sequence analysis of the amplicons demonstrated that the piroplasms present in the blood meal belonged to the Theileria orientalis group. This study demonstrates how xenosurveillance can be applied to detecting pathogens in livestock and confirms the presence of Theileria species in livestock from the United Kingdom.

Detection of Theileria luwenshuni in sheep from Great Britain.

BACKGROUND: Theileria spp. are tick-borne protozoan parasites of the Phylum Apicomplexa, Order Piroplasmida that infect a wide range of wild and domestic animals. In Great Britain, Theileria spp. have been reported from livestock associated with transmission by the tick Haemaphysalis punctata. However, these reports have not been associated with disease. This study has investigated the cause of a disease outbreak accompanied by mortality in a flock of sheep grazing reclaimed marshland in north Kent. FINDINGS: A polymerase chain reaction-reverse line blot assay indicated the presence of Theileria spp. in blood samples from five animals. Subsequent testing with a pan-piroplasm PCR of a larger panel of blood samples detected a piroplasm amplicon in 19 of 21 sheep submitted from the affected flock. Automated sequencing confirmed that these amplicons shared 99-100% identity with T. luwenshuni. CONCLUSIONS: The clinical and PCR data suggest infection with T. luwenshuni was associated with disease and mortality in this flock.