Alexander G.C. Vaux

European Surveillance for West Nile Virus in Mosquito Populations

A wide range of arthropod-borne viruses threaten both human and animal health either through their presence in Europe or through risk of introduction. Prominent among these is West Nile virus (WNV), primarily an avian virus, which has caused multiple outbreaks associated with human and equine mortality. Endemic outbreaks of West Nile fever have been reported in Italy, Greece, France, Romania, Hungary, Russia and Spain, with further spread expected. Most outbreaks in Western Europe have been due to infection with WNV Lineage 1. In Eastern Europe WNV Lineage 2 has been responsible for human and bird mortality, particularly in Greece, which has experienced extensive outbreaks over three consecutive years. Italy has experienced co-circulation with both virus lineages. The ability to manage this threat in a cost-effective way is dependent on early detection. Targeted surveillance for pathogens within mosquito populations offers the ability to detect viruses prior to their emergence in livestock, equine species or human populations. In addition, it can establish a baseline of mosquito-borne virus activity and allow monitoring of change to this over time. Early detection offers the opportunity to raise disease awareness, initiate vector control and preventative vaccination, now available for horses, and encourage personal protection against mosquito bites. This would have major benefits through financial savings and reduction in equid morbidity/mortality. However, effective surveillance that predicts virus outbreaks is challenged by a range of factors including limited resources, variation in mosquito capture rates (too few or too many), difficulties in mosquito identification, often reliant on specialist entomologists, and the sensitive, rapid detection of viruses in mosquito pools. Surveillance for WNV and other arboviruses within mosquito populations varies between European countries in the extent and focus of the surveillance. This study reviews the current status of WNV in mosquito populations across Europe and how this is informing our understanding of virus epidemiology. Key findings such as detection of virus, presence of vector species and invasive mosquito species are summarized, and some of the difficulties encountered when applying a cost-effective surveillance programme are highlighted.

Importation of Hyalomma marginatum, vector of Crimean-Congo haemorrhagic fever virus, into the United Kingdom by migratory birds.

Hyalomma marginatum ticks are an important vector of Crimean-Congo haemorrhagic fever virus which can result in a severe and potentially fatal disease in humans. Given the continued emergence of clinical cases in Eurasia and focalised upsurges of H. marginatum populations in Europe, it seemed prudent to assess the potential of this vector species to be introduced into the United Kingdom. Immature forms of H. marginatum are frequent ectoparasites of passerine birds many of which migrate from Africa to the UK each spring. Incoming birds were inspected for ticks during the spring migration in 2010 and 2011. A total of 68 ticks was collected from 971 birds (29 bird species), 21% (14) of the ticks were identified as H. marginatum. Oenanthe oenanthe (Northern wheatear) and Sylvia communis (Whitethroat) were found to be infested by this tick in both years and with multiple ticks. Single specimens were also removed from Acrocephalus schoenobaenus (Sedge warbler) and Phoenicurus phoenicurus (Common redstart) in 2010. This study provides the first contemporary evidence for substantial importation of this tick species into the UK.

Approaches to passive mosquito surveillance in the EU

The recent emergence in Europe of invasive mosquitoes and mosquito-borne disease associated with both invasive and native mosquito species has prompted intensified mosquito vector research in most European countries. Central to the efforts are mosquito monitoring and surveillance activities in order to assess the current species occurrence, distribution and, when possible, abundance, in order to permit the early detection of invasive species and the spread of competent vectors. As active mosquito collection, e.g. by trapping adults, dipping preimaginal developmental stages or ovitrapping, is usually cost-, time- and labour-intensive and can cover only small parts of a country, passive data collection approaches are gradually being integrated into monitoring programmes. Thus, scientists in several EU member states have recently initiated programmes for mosquito data collection and analysis that make use of sources other than targeted mosquito collection. While some of them extract mosquito distribution data from zoological databases established in other contexts, community-based approaches built upon the recognition, reporting, collection and submission of mosquito specimens by citizens are becoming more and more popular and increasingly support scientific research. Based on such reports and submissions, new populations, extended or new distribution areas and temporal activity patterns of invasive and native mosquito species were found. In all cases, extensive media work and communication with the participating individuals or groups was fundamental for success. The presented projects demonstrate that passive approaches are powerful tools to survey the mosquito fauna in order to supplement active mosquito surveillance strategies and render them more focused. Their ability to continuously produce biological data permits the early recognition of changes in the mosquito fauna that may have an impact on biting nuisance and the risk of pathogen transmission associated with mosquitoes. International coordination to explore synergies and increase efficiency of passive surveillance programmes across borders needs to be established.

West Nile virus vector Culex modestus established in southern England

BackgroundThe risk posed to the United Kingdom by West Nile virus (WNV) has previously been considered low, due to the absence or scarcity of the main Culex sp. bridge vectors. The mosquito Culex modestus is widespread in southern Europe, where it acts as the principle bridge vector of WNV. This species was not previously thought to be present in the United Kingdom.FindingsMosquito larval surveys carried out in 2010 identified substantial populations of Cx. modestus at two sites in marshland in southeast England. Host-seeking-adult traps placed at a third site indicate that the relative seasonal abundance of Cx. modestus peaks in early August. DNA barcoding of these specimens from the United Kingdom and material from southern France confirmed the morphological identification.ConclusionsCx. modestus appears to be established in the North Kent Marshes, possibly as the result of a recent introduction. The addition of this species to the United Kingdoms mosquito fauna may increase the risk posed to the United Kingdom by WNV.

Distribution of West Nile virus vector, Culex modestus, in England

Culex modestus is considered the main bridge vector of West Nile virus in continental Europe, responsible for transmitting virus from birds to humans (Balenghein and others 2008). Historically in the UK, this species was only reported in and around Portsmouth in 1944, with no further records (Marshall 1945). Consequently, assessments of public health risk from West Nile virus (WNV) in the UK were based upon the assumption that this key bridge …

Ticks and Borrelia in urban and peri-urban green space habitats in a city in southern England.

Ticks are becoming increasingly recognised as important vectors of pathogens in urban and peri-urban areas, including green space used for recreational activities. In the UK, the risk posed by ticks in such areas is largely unknown. In order to begin to assess the risk of ticks in urban/peri-urban areas in southern England, questing ticks were collected from five different habitat types (grassland, hedge, park, woodland and woodland edge) in a city during the spring, summer and autumn of 2013/2014 and screened for Borrelia burgdorferi sensu lato. In addition, seasonal differences in B. burgdorferi s.l. prevalence were also investigated at a single site during 2015. Ixodes ricinus presence and activity were significantly higher in woodland edge habitat and during spring surveys. DNA of Borrelia burgdorferi s.l. was detected in 18.1% of nymphs collected across the 25 sites during 2013 and 2014 and two nymphs also tested positive for the newly emerging tick-borne pathogen B. miyamotoi. Borrelia burgdorferi s.l. prevalence at a single site surveyed in 2015 were found to be significantly higher during spring and summer than in autumn, with B. garinii and B. valaisiana most commonly detected. These data indicate that a range of habitats within an urban area in southern England support ticks and that urban Borrelia transmission cycles may exist in some of the urban green spaces included in this study. Sites surveyed were frequently used by humans for recreational activities, providing opportunity for exposure to Borrelia infected ticks in an urban/peri-urban space that might not be typically associated with tick-borne disease transmission.

Colonization of UK coastal realignment sites by mosquitoes: implications for design, management, and public health

ABSTRACT: Coastal realignment is now widely instituted in the UK as part of local flood risk management plans to compensate for the loss of European protected habitat and to mitigate the effects of sea-level rise and coastal squeeze. Coastal aquatic habitats have long been known to provide suitable habitats for brackish-water mosquitoes and historically, coastal marshes were considered to support anopheline mosquito populations that were responsible for local malaria transmission. This study surveyed the eight largest managed realignment (MRA) sites in England (Essex and the Humber) for mosquito habitats. The apparent absence of anopheline mosquitoes exploiting aquatic habitats at all of these sites suggests that the risk of malaria associated with MRA sites is currently negligible. However, three of the eight sites supported populations of two nuisance and potential arboviral vector species, Aedes detritus and Aedes caspius. The aquatic habitats that supported mosquitoes resulted from a) specific design aspects of the new sea wall (ballast to mitigate wave action and constructed saline borrow ditches) that could be designed out or managed or b) isolated pools created through silt accretion or expansion of flooded zones to neighbouring pasture. The public health risks and recommendations for management are discussed in this report. This report highlights the need for pro-active public health impact assessments prior to MRA development in consultation with the Health Protection Agency, as well as the need for a case-by-case approach to design and management to mitigate mosquito or mosquito-borne disease issues now and in the future.

Impacts of the creation, expansion and management of English wetlands on mosquito presence and abundance – developing strategies for future disease mitigation

The incidence of mosquito-borne diseases is increasing in Europe, partly due to the incursion of a number of invasive species known to be vectors of dengue and chikungunya viruses, but also due to the involvement of native species in the transmission of West Nile virus and malaria. For some of these pathogens, there is a risk of the re-emergence of vector-borne diseases that were once widespread in Europe, but declined partly due to large-scale land-drainage projects. Some mosquito species exploit container habitats as breeding sites in urban areas; an adaptation to human-made micro-habitats resulting from increased urbanisation. However, many species thrive in natural wetland ecosystems. Owing to the impacts of climate change there is an urgent need for environmental adaptation, such as the creation of new wetlands to mitigate coastal and inland flooding. In some cases, these initiatives can be coupled with environmental change strategies to protect a range of endangered flora and fauna species by enhancing and extending wetland landscapes, which may by driven by European legislation, particularly in urban areas. This paper reviews field studies conducted in England to assess the impact of newly created wetlands on mosquito colonisation in a) coastal, b) urban and c) arable reversion habitats. It also considers the impact of wetland management on mosquito populations and explores the implications of various water and vegetation management options on the range of British mosquito species. Understanding the impact of wetland creation and management strategies on mosquito prevalence and the potential risk of increasing the levels of nuisance or disease vector species will be crucial in informing health and well-being risk assessments, guiding targeted control, and anticipating the social effects of extreme weather and climate change. Although new wetlands will certainly extend aquatic habitats for mosquitoes, not all species will become a major nuisance or a vector concern as a result. Understanding how the design and management of wetlands might exacerbate mosquito densities is crucial if we are to manage nuisance mosquitoes and control vector species in the event of a disease outbreak. This entomological evidence-base will ensure that control strategies achieve optimal efficacy at minimal cost.

Enhanced West Nile virus surveillance in the North Kent marshes, UK

BackgroundAs part of efforts to more fully understand the potential risks posed by West Nile virus (WNV) and Usutu virus (USUV) in the UK, and following on from previous reports of a potential bridge vector Culex modestus for these viruses, at wetland sites in North Kent, mosquito surveillance was undertaken more widely across the Isle of Sheppey, the Hoo Peninsula and the Kent mainland.MethodsLarval surveys were conducted and Mosquito Magnet® adult traps were used to collect adult mosquitoes. Pools of female mosquitoes were tested for the presence of WNV using real-time reverse transcriptase polymerase chain reaction. A subset of samples was tested for USUV.ResultsCulex modestus was found in both the pre-imaginal and imago stage at all five locations surveyed, accounting for 90% of adult mosquitoes collected. WNV or USUV were not detected in any sample.ConclusionsAlthough no mosquitoes have been shown to be virus positive, the field survey data from this study demonstrated the dominance of an important bridge vector species for WNV in this region. Its wide geographical distribution highlights the need to update risk assessments on WNV introduction, and to maintain vigilance for WNV in the South East of England.

Colonization of a Newly Constructed Urban Wetland by Mosquitoes in England: Implications for Nuisance and Vector Species

ABSTRACT: Urban wetlands are being created in the UK as part of sustainable urban drainage strategies, to create wetland habitats lost during development, to provide a habitat for protected species, and to increase the publics access to ‘blue-space’ for the improvement of health and well-being. Sewage treatment reedbeds are also being incorporated into newly constructed wetlands to offer an alternative approach to dealing with sewage. This field study aims to provide the first UK evidence of how such newly constructed aquatic habitats are colonized by mosquitoes. A number of new aquatic habitats were surveyed for immature mosquitoes every fortnight over the first two years following wetland construction. The majority of mosquitoes collected were Culex sp. and were significantly associated with the sewage treatment reedbed system, particularly following storm events and sewage inflow. Other more natural aquatic habitats that were subject to cycles of drying and re-wetting contributed the majority of the remaining mosquitoes colonizing. Colonization of permanent habitats was slow, particularly where fluctuations in water levels inhibited emergent vegetation growth. It is recommended that during the planning process for newly constructed wetlands consideration is given on a case-by-case basis to the impact of mosquitoes, either as a cause of nuisance or as potential vectors. Although ornithophagic Culex dominated in this wetland, their potential role as enzootic West Nile virus vectors should not be overlooked.