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Possible Ecology and Epidemiology of Medically Important Mosquito-Borne Arboviruses in Great Britain

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Possible Ecology and Epidemiology of Medically Important Mosquito-Borne Arboviruses in Great Britain Epidemiol. Infect. (2007), 135, 466–482. f 2006 Cambridge University Press doi:10.1017/S0950268806007047 Printed in the United Kingdom Possible ecology and epidemiology of medically important mosquito-borne arboviruses in Great Britain J. M. MEDLOCK 1*, K. R. SNOW 2 AND S. LEACH1 1 Health Protection Agency, Centre for Emergency Preparedness & Response, Porton Down, Salisbury, Wiltshire, UK 2 School of Health & Bioscience, University of East London, London, UK (Accepted 30 May 2006; first published online 8 August 2006) SUMMARY Nine different arboviruses are known to be transmitted by, or associated with, mosquitoes in Europe, and several (West Nile, Sindbis and Tahyna viruses) are reported to cause outbreaks of human disease. Although there have been no reported human cases in Great Britain (GB), there have been no published in-depth serological surveys for evidence of human infection. This paper investigates the ecological and entomological factors that could influence or restrict transmission of these viruses in GB, suggesting that in addition to West Nile virus, Sindbis and Tahyna viruses could exist in enzootic cycles, and that certain ecological factors could facilitate transmission to humans. However, the level of transmission is likely to be lower than in endemic foci elsewhere in Europe due to key ecological differences related to spatial and temporal dynamics of putative mosquito vectors and presence of key reservoir hosts. Knowledge of the potential GB-specific disease ecology can aid assessments of risk from mosquito-borne arboviruses. INTRODUCTION endemic in Europe [1–3], with suggestions that they may occur enzootically in the United Kingdom (UK) There is currently considered to be no transmission [4]. Following the large-scale outbreak of West Nile of mosquito-borne arboviruses to humans in Great virus (WNV) in North America and recent outbreaks Britain (GB), despite a number of mosquito-borne in Romania, Russia, Israel and France, an inves- arboviruses being endemic in other parts of Europe, tigation into the presence of mosquito-borne viruses where they cause human disease. However, to date in GB was conducted, resulting in evidence of no in-depth serological surveys for mosquito-borne neutralizing antibodies to WNV, Sindbis virus and viruses in the GB human population have been pub- Usutu virus in British resident birds [5]. Prior to lished, and therefore an assessment of their possible this, the only previous record of a mosquito-borne ecology and epidemiology is required to aid under- arbovirus in GB was serological evidence of Tahyna standing as to whether these viruses already exist virus in small mammals in Devon [6]. The recent enzootically in GB and whether they could be associ- spread of WNV across North America, coupled with ated with human infection. seropositivity in British resident birds have led to A number of papers have reviewed the known the development of UK contingency plans for WNV transmission dynamics of mosquito-borne arboviruses [7] and vector control [8]. The occurrence and abundance of mosquito vector * Author for correspondence: Jolyon Medlock, Health species, or potential vector species, is a prerequisite Protection Agency, Centre for Emergency Preparedness & Response, Porton Down, Salisbury, Wiltshire SP4 0JG, UK. for enzootic transmission of mosquito-borne viruses (Email: [email protected]) in GB. Thirty-three mosquito species have been Downloaded from https://www.cambridge.org/core. IP address: 170.106.202.58, on 01 Oct 2021 at 21:39:54, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0950268806007047 Mosquito-borne arboviruses in Great Britain 467 recorded in GB (Table 1): six species of Anophelinae Sindbis virus (SINV) (genus Anopheles) and 27 species of Culicinae in seven genera: Aedes (2), Ochlerotatus (11), Finlaya SINV (Togaviridae: Alphavirus) was first isolated (1), Coquillettidia (1), Culex (4), Culiseta (7), and from Cx. univittatus near Sindbis village, Egypt in Orthopodomyia (1). Several species (Ae. vexans, An. 1952, with the first human case reported in Uganda algeriensis, Cx. modestus, Cs. longiareolata, Cs. alas- in 1961. SINV has since been isolated from Africa, kaensis, Oc. communis, Oc. leucomelas, Oc. sticticus Europe, Middle East, Asia and Australia; however, it and Or. pulcripalpis) are either rare, adopt localized only appears to be clinically apparent in northern distributions or have only historically occurred in Europe (mainly 60x–64x N) and in South Africa [14]. GB and can therefore be generally discounted from In Scandinavia, infection with SINV or SIN-like eco-epidemiological studies of mosquito-borne arbo- viruses is known by different names in different virus transmission in GB. An ecological understand- regions: Ockelbo disease in Sweden, Karelian fever ing of candidate mosquito vectors of arboviruses is in western Russia, and Pogosta disease in Finland. an important aspect of surveillance and aids assess- There have been no fatal human cases reported ment of likely spatio-temporal dynamics of trans- and many SIN or SIN-like virus infections are mod- mission and associated public health risks. A detailed erate or mild, especially in children and adolescents, review of the ecology of candidate WNV mosquito so the potential exists for under-reporting and/or vectors in the British Isles based upon known vector under-diagnosis [15]. There appears to be more sub- status in continental Europe and host preferences of clinical infections than clinical cases with reported endemic species has been published [9]. The main aims ratios of 20:1 to 40:1 in Sweden and 17:1 in Finland of this paper are to assess the ecological potential for [16, 17]. However, where clinical disease in humans transmission of other mosquito-borne arboviruses does occur the infection is characterized by fever, in GB and associated public health concerns and rash and arthritis, with non-pruritic skin lesions secondly, by incorporating data on distribution from beginning as macules, which become papular and the British mosquito recording scheme to identify progress to central vesicle formation, which are, areas for possible transmission and more importantly occasionally, haemorrhagic [18]. Arthralgias occur targeted surveillance of potentially medically import- in large and small joints, particularly ankles, wrists ant arboviruses including WNV#. and knees [19] and may be so severe as to be immobilizing [20] with moderate joint pain and stiff- Mosquito-borne arboviruses in Europe ness persisting for months or years, with chronic joint (or muscle) problems occurring in y20% of Up to 1996, eight arboviruses transmitted by, or cases [20]. Following the first human case in Sweden associated with, mosquitoes had been recorded in in the 1960s, Ockelbo disease was responsible for Europe (Table 2; [2]) including: members of the considerable morbidity in Scandinavia during the Togaviridae (Sindbis), Flaviviridae (West Nile, 1980s. In 1981, the Russian federation and Finland dengue), and Bunyaviridae (Batai, Inkoo, Lednice, reported 200 and 300 laboratory-confirmed cases Tahyna and Uukuniemi); Usutu virus has since been of Karelian fever and Pogosta disease respectively added to this list [13]. Five of these arboviruses are [21]. The largest Pogosta disease outbreak occurred generally associated with human disease in Europe: in Finland in 1995 with 400 confirmed cases. Annual Sindbis, West Nile, Tahyna, Batai and Inkoo. The incidence rates in endemic regions of affected public health concerns for GB will now be considered countries range from 2.7/100 000 in Finland, 2.9/ in more depth. 100 000 in Sweden to 18/100 000 in northern Karelia [16, 17]. Epidemics can involve hundreds of people, # Although currently available distribution maps do not represent and in these epidemic years, the number of cases may a complete picture of the distribution of British mosquitoes [10], be 10 times higher than in non-epidemic years. The they provide, through the combination of recorded distributions of potential vectors, an insight into areas where transmission might annual number of cases in Finland from 1980 to 1996 occur and therefore assist in targeting surveillance of arboviral ranged from 1 to 1282 [17]. Human disease normally transmission. It should be borne in mind, however, that other areas not illustrated on these maps could be suitable for transmission of appears at the end of July or beginning of August, these arboviruses and the development of geospatial risk maps peaks in late August with few cases from October [16]. would be useful. However, incorporating a number of different mosquito species that favour a variety of diverse ecologies would be A virus closely related to SINV (Ockelbo virus) was complex. first isolated from mosquitoes of the genus Culiseta Downloaded from https://www.cambridge.org/core. IP address: 170.106.202.58, on 01 Oct 2021 at 21:39:54, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0950268806007047 https://www.cambridge.org/core/terms Downloaded from https://www.cambridge.org/core 468 J. M. Medlock, K. R. Snow and S. Leach . https://doi.org/10.1017/S0950268806007047 Table 1. Mosquitoes recorded from Great Britain (after [9]) . IPaddress: Preferred aquatic Preferred aquatic habitat in Great habitat in Great Species Occurrence [10, 11] Britain Species Occurrence [10, 11] Britain 170.106.202.58 Aedes cinereus Widespread, patchy Flooded
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