Publications by authors named "Simon Carpenter"

64 Publications

Culicoides imicola (Biting Midge).

Trends Parasitol 2021 May 26;37(5):458-459. Epub 2021 Mar 26.

ASTRE, Univ Montpellier, CIRAD, INRAE, Montpellier, France.

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http://dx.doi.org/10.1016/j.pt.2021.03.001DOI Listing
May 2021

Thermal limits for flight activity of field-collected Culicoides in the United Kingdom defined under laboratory conditions.

Parasit Vectors 2021 Jan 18;14(1):55. Epub 2021 Jan 18.

The Pirbright Institute, Ash Road, Woking, GU24 0NF, UK.

Background: Culicoides biting midges (Diptera: Ceratopogonidae) are biological vectors of internationally important arboviruses and inflict biting nuisance on humans, companion animals and livestock. In temperate regions, transmission of arboviruses is limited by temperature thresholds, in both replication and dissemination of arboviruses within the vector and in the flight activity of adult Culicoides. This study aims to determine the cold-temperature thresholds for flight activity of Culicoides from the UK under laboratory conditions.

Methods: Over 18,000 Culicoides adults were collected from the field using 4 W down-draught miniature ultraviolet Centers for Disease Control traps. Populations of Culicoides were sampled at three different geographical locations within the UK during the summer months and again in the autumn at one geographical location. Activity at constant temperatures was assessed using a bioassay that detected movement of adult Culicoides towards an ultraviolet light source over a 24-h period.

Results: The proportion of active adult Culicoides increased with temperature but cold temperature thresholds for activity varied significantly according to collection season and location. Populations dominated by the subgenus Avaritia collected in South East England had a lower activity threshold temperature in the autumn (4 °C) compared with populations collected in the summer (10 °C). Within the subgenus Avaritia, Culicoides scoticus was significantly more active across all temperatures tested than Culicoides obsoletus within the experimental setup. Populations of Culicoides impunctatus collected in the North East of England were only active once temperatures reached 14 °C. Preliminary data suggested flight activity of the subgenus Avaritia does not differ between populations in South East England and those in the Scottish Borders.

Conclusions: These findings demonstrate seasonal changes in temperature thresholds for flight and across different populations of Culicoides. These data, alongside that defining thresholds for virus replication within Culicoides, provide a primary tool for risk assessment of arbovirus transmission in temperate regions. In addition, the study also provides a comparison with thermal limits derived directly from light-suction trapping data, which is currently used as the main method to define adult Culicoides activity during surveillance.
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http://dx.doi.org/10.1186/s13071-020-04552-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7814454PMC
January 2021

Investigation of bovine ephemeral fever virus transmission by putative dipteran vectors under experimental conditions.

Parasit Vectors 2020 Nov 26;13(1):597. Epub 2020 Nov 26.

The Pirbright Institute, Pirbright, Surrey, GU24 0NF, UK.

Background: Bovine ephemeral fever virus (Rhabdoviridae: Ephemerovirus) (BEFV) causes bovine ephemeral fever (BEF), an economically important disease of cattle and water buffalo. Outbreaks of BEF in Africa, Australia, Asia and the Middle East are characterized by high rates of morbidity and highly efficient transmission between cattle hosts. Despite this, the vectors of BEFV remain poorly defined.

Methods: Colony lines of biting midges (Culicoides sonorensis) and mosquitoes (Aedes aegypti, Culex pipiens and Culex quinquefasciatus) were infected with a strain of BEFV originating from Israel by feeding on blood-virus suspensions and by intrathoracic inoculation. In addition, in vivo transmission of BEFV was also assessed by allowing C. sonorensis inoculated by the intrathoracic route to feed on male 6 month-old Holstein-Friesian calves.

Results: There was no evidence of BEFV replication within mosquitoes fed on blood/virus suspensions for mosquitoes of any species tested for each of the three colony lines. In 170 C. sonorensis fed on the blood/virus suspension, BEFV RNA was detected in the bodies of 13 individuals and in the heads of two individuals, indicative of fully disseminated infections and an oral susceptibility rate of 1.2%. BEFV RNA replication was further demonstrated in all C. sonorensis that were inoculated by the intrathoracic route with virus after 5, 6 or 7 days post-infection. Despite this, transmission of BEFV could not be demonstrated when infected C. sonorensis were allowed to feed on calves.

Conclusions: No evidence for infection or dissemination of BEFV (bovine/Israel/2005-6) in mosquitoes of three different species was found. Evidence was found for infection of C. sonorensis by the oral route. However, attempts to transmit BEFV to calves from infected C. sonorensis failed. These results highlight the challenge of defining the natural vector of BEFV and of establishing an in vivo transmission model. The results are discussed with reference to the translation of laboratory-based studies to inference of vector competence in the field.
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http://dx.doi.org/10.1186/s13071-020-04485-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7690080PMC
November 2020

Risk-based surveillance for bluetongue virus in cattle on the south coast of England in 2017 and 2018.

Vet Rec 2020 Nov 11;187(11):e96. Epub 2020 Sep 11.

Entomology, The Pirbright Institute, Pirbright, Surrey, UK.

Background: Bluetongue (BT) is a viral disease of ruminants and camelids which can have a significant impact on animal health and welfare and cause severe economic loss. The UK has been officially free of bluetongue virus (BTV) since 2011. In 2015, BTV-8 re-emerged in France and since then BTV has been spreading throughout Europe. In response to this outbreak, risk-based active surveillance was carried out at the end of the vector seasons in 2017 and 2018 to assess the risk of incursion of BTV into Great Britain.

Method: Atmospheric dispersion modelling identified counties on the south coast of England at higher risk of an incursion. Blood samples were collected from cattle in five counties based on a sample size designed to detect at least one positive if the prevalence was 5 per cent or greater, with 95 per cent confidence.

Results: No virus was detected in the 478 samples collected from 32 farms at the end of the 2017 vector season or in the 646 samples collected from 43 farms at the end of the 2018 vector season, when tested by RT-qPCR.

Conclusion: The negative results from this risk-based survey provided evidence to support the continuation of the UK's official BTV-free status.
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http://dx.doi.org/10.1136/vr.106016DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7786256PMC
November 2020

Outbreak of African horse sickness in Thailand, 2020.

Transbound Emerg Dis 2020 Jun 27. Epub 2020 Jun 27.

The Pirbright Institute, Pirbright, UK.

African horse sickness was confirmed in horses in Thailand during March 2020. The virus was determined to belong to serotype 1 and is phylogenetically closely related to isolates from South Africa. This is the first incidence of African horse sickness occurring in South East Asia and of serotype 1 outside of Africa.
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http://dx.doi.org/10.1111/tbed.13701DOI Listing
June 2020

Diversity of Transmission Outcomes Following Co-Infection of Sheep with Strains of Bluetongue Virus Serotype 1 and 8.

Microorganisms 2020 Jun 5;8(6). Epub 2020 Jun 5.

The Pirbright Institute, Pirbright, Surrey GU24 0NF, UK.

Bluetongue virus (BTV) causes an economically important disease, bluetongue (BT), in susceptible ruminants and is transmitted primarily by species of biting midges (Diptera: Ceratopogonidae). Since 2006, northern Europe has experienced multiple incursions of BTV through a variety of routes of entry, including major outbreaks of strains of BTV serotype 8 (BTV-8) and BTV serotype 1 (BTV-1), which overlapped in distribution within southern Europe. In this paper, we examined the variation in response to coinfection with strains of BTV-1 and BTV-8 using an in vivo transmission model involving , low passage virus strains, and sheep sourced in the United Kingdom. In the study, four sheep were simultaneously infected using BTV-8 and BTV-1 intrathoracically inoculated and co-infections of all sheep with both strains were established. However, there were significant variations in both the initiation and peak levels of virus RNA detected throughout the experiment, as well as in the infection rates in the that were blood-fed on experimentally infected sheep at peak viremia. This is discussed in relation to the potential for reassortment between these strains in the field and the policy implications for detection of BTV strains.
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http://dx.doi.org/10.3390/microorganisms8060851DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7356686PMC
June 2020

Continuous Cell Lines from the European Biting Midge (Meigen, 1830).

Microorganisms 2020 May 30;8(6). Epub 2020 May 30.

School of Veterinary Medicine and Science, University of Nottingham, Sutton Bonington Campus, LE12 5RD, UK.

biting midges (Diptera: Ceratopogonidae) transmit arboviruses of veterinary or medical importance, including bluetongue virus (BTV) and Schmallenberg virus, as well as causing severe irritation to livestock and humans. Arthropod cell lines are essential laboratory research tools for the isolation and propagation of vector-borne pathogens and the investigation of host-vector-pathogen interactions. Here we report the establishment of two continuous cell lines, CNE/LULS44 and CNE/LULS47, from embryos of , a midge distributed throughout the Western Palearctic region. Species origin of the cultured cells was confirmed by polymerase chain reaction (PCR) amplification and sequencing of a fragment of the gene, and the absence of bacterial contamination was confirmed by bacterial 16S rRNA PCR. Both lines have been successfully cryopreserved and resuscitated. The majority of cells examined in both lines had the expected diploid chromosome number of 2 = 6. Transmission electron microscopy of CNE/LULS44 cells revealed the presence of large mitochondria within cells of a diverse population, while arrays of virus-like particles were not seen. CNE/LULS44 cells supported replication of a strain of BTV serotype 1, but not of a strain of serotype 26 which is not known to be insect-transmitted. These new cell lines will expand the scope of research on -borne pathogens.
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http://dx.doi.org/10.3390/microorganisms8060825DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7356041PMC
May 2020

The tree that hides the forest: cryptic diversity and phylogenetic relationships in the Palaearctic vector Obsoletus/Scoticus Complex (Diptera: Ceratopogonidae) at the European level.

Parasit Vectors 2020 May 20;13(1):265. Epub 2020 May 20.

National Veterinary Research Institute, Puławy, Poland.

Background: Culicoides obsoletus is an abundant and widely distributed Holarctic biting midge species, involved in the transmission of bluetongue virus (BTV) and Schmallenberg virus (SBV) to wild and domestic ruminants. Females of this vector species are often reported jointly with two morphologically very close species, C. scoticus and C. montanus, forming the Obsoletus/Scoticus Complex. Recently, cryptic diversity within C. obsoletus was reported in geographically distant sites. Clear delineation of species and characterization of genetic variability is mandatory to revise their taxonomic status and assess the vector role of each taxonomic entity. Our objectives were to characterize and map the cryptic diversity within the Obsoletus/Scoticus Complex.

Methods: Portion of the cox1 mitochondrial gene of 3763 individuals belonging to the Obsoletus/Scoticus Complex was sequenced. Populations from 20 countries along a Palaearctic Mediterranean transect covering Scandinavia to Canary islands (North to South) and Canary islands to Turkey (West to East) were included. Genetic diversity based on cox1 barcoding was supported by 16S rDNA mitochondrial gene sequences and a gene coding for ribosomal 28S rDNA. Species delimitation using a multi-marker methodology was used to revise the current taxonomic scheme of the Obsoletus/Scoticus Complex.

Results: Our analysis showed the existence of three phylogenetic clades (C. obsoletus clade O2, C. obsoletus clade dark and one not yet named and identified) within C. obsoletus. These analyses also revealed two intra-specific clades within C. scoticus and raised questions about the taxonomic status of C. montanus.

Conclusions: To our knowledge, our study provides the first genetic characterization of the Obsoletus/Scoticus Complex on a large geographical scale and allows a revision of the current taxonomic classification for an important group of vector species of livestock viruses in the Palaearctic region.
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http://dx.doi.org/10.1186/s13071-020-04114-1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7238629PMC
May 2020

Culicoides species composition and molecular identification of host blood meals at two zoos in the UK.

Parasit Vectors 2020 Mar 16;13(1):139. Epub 2020 Mar 16.

The Pirbright Institute, Ash Road, Woking, Surrey, GU24 0NF, UK.

Background: Culicoides biting midges are biological vectors of arboviruses including bluetongue virus (BTV), Schmallenberg virus (SBV) and African horse sickness virus (AHSV). Zoos are home to a wide range of 'at risk' exotic and native species of animals. These animals have a high value both in monetary terms, conservation significance and breeding potential. To understand the risk these viruses pose to zoo animals, it is necessary to characterise the Culicoides fauna at zoos and determine which potential vector species are feeding on which hosts.

Methods: Light-suction traps were used at two UK zoos: the Zoological Society of London (ZSL) London Zoo (LZ) and ZSL Whipsnade Zoo (WZ). Traps were run one night each week from June 2014 to June 2015. Culicoides were morphologically identified to the species level and any blood-fed Culicoides were processed for blood-meal analysis. DNA from blood meals was extracted and amplified using previously published primers. Sequencing was then carried out to determine the host species.

Results: A total of 11,648 Culicoides were trapped and identified (n = 5880 from ZSL WZ; n = 5768 from ZSL LZ), constituting 25 different species. The six putative vectors of BTV, SBV and AHSV in northern Europe were found at both zoos and made up the majority of the total catch (n = 10,701). A total of 31 host sequences were obtained from blood-fed Culicoides. Culicoides obsoletus/C. scoticus, Culicoides dewulfi, Culicoides parroti and Culicoides punctatus were found to be biting a wide range of mammals including Bactrian camels, Indian rhinoceros, Asian elephants and humans, with Culicoides obsoletus/C. scoticus also biting Darwin's rhea. The bird-biting species, Culicoides achrayi, was found to be feeding on blackbirds, blue tits, magpies and carrion crows.

Conclusions: To our knowledge, this is the first study to directly confirm blood-feeding of Culicoides on exotic zoo animals in the UK and shows that they are able to utilise a wide range of exotic as well as native host species. Due to the susceptibility of some zoo animals to Culicoides-borne arboviruses, this study demonstrates that in the event of an outbreak of one of these viruses in the UK, preventative and mitigating measures would need to be taken.
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http://dx.doi.org/10.1186/s13071-020-04018-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7076997PMC
March 2020

Complete Genome Sequence of a Bovine Ephemeral Fever Virus Isolate from Israel.

Microbiol Resour Announc 2019 Oct 10;8(41). Epub 2019 Oct 10.

Animal and Plant Health Agency, Addlestone, Surrey, United Kingdom.

Here, we report the first complete genome of a bovine ephemeral fever virus (BEFV) isolate from an infected bovine in Israel. The genome shares 95.3% identity with a Turkish genomic sequence but contains α3 and γ open reading frames that are truncated compared to those of existing BEFV genome sequences.
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http://dx.doi.org/10.1128/MRA.00822-19DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6787318PMC
October 2019

Long-term shifts in the seasonal abundance of adult biting midges and their impact on potential arbovirus outbreaks.

J Appl Ecol 2019 Jul 29;56(7):1649-1660. Epub 2019 May 29.

The Pirbright Institute Pirbright UK.

Surveillance of adult biting midge flight activity is used as an applied ecological method to guide the management of arbovirus incursions on livestock production in Europe and Australia.To date the impact of changes in the phenology of adult vector activity on arbovirus transmission has not been defined. We investigated this at two sites in the UK, identifying 150,000 biting midges taken from 2867 collections over a nearly 40 year timescale.Whilst we recorded no change in seasonal activity at one site, shifts in first adult appearance and last adult appearance increased the seasonal activity period of species at the other site by 40 days over the time period.Lengthening of the adult activity season was driven by an increase in abundance of and correlated with local increases in temperature and precipitation. This diversity in responses poses significant challenges for predicting future transmission and overwintering risk. Our analysis not only shows a dramatic and consistent increase in the adult active period of biting midges, but also that this varies significantly between sites. This suggests broad-scale analyses alone are insufficient to understand the potential impacts of changes in climate on arbovirus vector populations. Understanding the impact of climate change on adult seasonality and transmission of arboviruses requires the context of changes in a range of other local ecological drivers.
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http://dx.doi.org/10.1111/1365-2664.13415DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6618056PMC
July 2019

Evidence of reduced viremia, pathogenicity and vector competence in a re-emerging European strain of bluetongue virus serotype 8 in sheep.

Transbound Emerg Dis 2019 May 22;66(3):1177-1185. Epub 2019 Feb 22.

The Pirbright Institute, Pirbright, UK.

The outbreak of bluetongue virus (BTV) serotype 8 (BTV-8) during 2006-2009 in Europe was the most costly epidemic of the virus in recorded history. In 2015, a BTV-8 strain re-emerged in France which has continued to circulate since then. To examine anecdotal reports of reduced pathogenicity and transmission efficiency, we investigated the infection kinetics of a 2007 UK BTV-8 strain alongside the re-emerging BTV-8 strain isolated from France in 2017. Two groups of eight BTV-naïve British mule sheep were inoculated with 5.75 log TCID /ml of either BTV-8 strain. BTV RNA was detected by 2 dpi in both groups with peak viraemia occurring between 5-9 dpi. A significantly greater amount of BTV RNA was detected in sheep infected with the 2007 strain (6.0-8.8 log genome copies/ml) than the re-emerging BTV-8 strain (2.9-7.9 log genome copies/ml). All infected sheep developed BTV-specific antibodies by 9 dpi. BTV was isolated from 2 dpi to 12 dpi for 2007 BTV-8-inoculated sheep and from 5 to 10 dpi for sheep inoculated with the remerging BTV-8. In Culicoides sonorensis feeding on the sheep over the period 7-12 dpi, vector competence was significantly higher for the 2007 strain than the re-emerging strain. Both the proportion of animals showing moderate (as opposed to mild or no) clinical disease (6/8 vs. 1/8) and the overall clinical scores (median 5.25 vs. 3) were significantly higher in sheep infected with the 2007 strain, compared to those infected with the re-emerging strain. However, one sheep infected with the re-emerging strain was euthanized at 16 dpi having developed severe lameness. This highlights the potential of the re-emerging BTV-8 to still cause illness in naïve ruminants with concurrent costs to the livestock industry.
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http://dx.doi.org/10.1111/tbed.13131DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6563110PMC
May 2019

The genome of the biting midge Culicoides sonorensis and gene expression analyses of vector competence for bluetongue virus.

BMC Genomics 2018 Aug 22;19(1):624. Epub 2018 Aug 22.

The Pirbright Institute, Ash Road, Woking, Surrey, GU24 0NF, UK.

Background: The new genomic technologies have provided novel insights into the genetics of interactions between vectors, viruses and hosts, which are leading to advances in the control of arboviruses of medical importance. However, the development of tools and resources available for vectors of non-zoonotic arboviruses remains neglected. Biting midges of the genus Culicoides transmit some of the most important arboviruses of wildlife and livestock worldwide, with a global impact on economic productivity, health and welfare. The absence of a suitable reference genome has hindered genomic analyses to date in this important genus of vectors. In the present study, the genome of Culicoides sonorensis, a vector of bluetongue virus (BTV) in the USA, has been sequenced to provide the first reference genome for these vectors. In this study, we also report the use of the reference genome to perform initial transcriptomic analyses of vector competence for BTV.

Results: Our analyses reveal that the genome is 189 Mb, assembled in 7974 scaffolds. Its annotation using the transcriptomic data generated in this study and in a previous study has identified 15,612 genes. Gene expression analyses of C. sonorensis females infected with BTV performed in this study revealed 165 genes that were differentially expressed between vector competent and refractory females. Two candidate genes, glutathione S-transferase (gst) and the antiviral helicase ski2, previously recognized as involved in vector competence for BTV in C. sonorensis (gst) and repressing dsRNA virus propagation (ski2), were confirmed in this study.

Conclusions: The reference genome of C. sonorensis has enabled preliminary analyses of the gene expression profiles of vector competent and refractory individuals. The genome and transcriptomes generated in this study provide suitable tools for future research on arbovirus transmission. These provide a valuable resource for these vector lineage, which diverged from other major Dipteran vector families over 200 million years ago. The genome will be a valuable source of comparative data for other important Dipteran vector families including mosquitoes (Culicidae) and sandflies (Psychodidae), and together with the transcriptomic data can yield potential targets for transgenic modification in vector control and functional studies.
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http://dx.doi.org/10.1186/s12864-018-5014-1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6106943PMC
August 2018

Sheep breed and shearing influences attraction and blood-feeding behaviour of Culicoides (Diptera: Ceratopogonidae) on a UK farm.

Parasit Vectors 2018 Aug 20;11(1):473. Epub 2018 Aug 20.

The Pirbright Institute, Pirbright, Surrey, UK.

Background: Culicoides biting midges (Diptera: Ceratopogonidae) are responsible for the biological transmission of arboviruses of international importance between ruminant livestock. These arboviruses include bluetongue virus (BTV) and Schmallenberg virus (SBV), which have emerged in unprecedented outbreaks in northern Europe. The impact of breed and shearing of sheep on Culicoides: host contact rates has not been investigated in detail and has the potential to influence arbovirus transmission and control measures employed to limit spread.

Methods: Attraction of Culicoides to Hartline and Hartline/Suffolk cross-breed sheep was compared using 224 drop trap collections over 22 nights and 181 catches from sheared or unsheared Hartline/Suffolk ewes were made over 17 nights to compare Culicoides activity and rates of blood engorgement.

Results: A total of 31,314 Culicoides was collected in the two trials and females of the subgenus Avaritia represented over 96.9% of individuals collected. Attraction to breed was dependent upon species of Culicoides and physiological status, with a significantly greater number of individuals collected on the cross-breed sheep. Shearing of sheep did not significantly increase or decrease the number of Culicoides attracted but increased the rate of successful engorgement.

Conclusions: Both breed and shearing were shown to influence Culicoides biting rate on sheep. These data are useful in a direct context in understanding the likely impact of control measures against arboviruses including BTV and SBV and additionally in providing data from field-based studies to enable modelling exercises of arbovirus transmission and spread.
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http://dx.doi.org/10.1186/s13071-018-3003-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6102838PMC
August 2018

Blood-feeding, susceptibility to infection with Schmallenberg virus and phylogenetics of Culicoides (Diptera: Ceratopogonidae) from the United Kingdom.

Parasit Vectors 2018 02 27;11(1):116. Epub 2018 Feb 27.

Vector-borne Viral Disease Programme, The Pirbright Institute, Pirbright, Surrey, UK.

Background: Culicoides biting midges (Diptera: Ceratopogonidae) are responsible for the biological transmission of internationally important arboviruses of livestock. In 2011, a novel Orthobunyavirus was discovered in northern Europe causing congenital malformations and abortions in ruminants. From field studies, Culicoides were implicated in the transmission of this virus which was subsequently named Schmallenberg virus (SBV), but to date no assessment of susceptibility to infection of field populations under standardised laboratory conditions has been carried out. We assessed the influence of membrane type (chick skin, collagen, Parafilm M®) when offered in conjunction with an artificial blood-feeding system (Hemotek, UK) on field-collected Culicoides blood-feeding rates. Susceptibility to infection with SBV following blood-feeding on an SBV-blood suspension provided via either (i) the Hemotek system or via (ii) a saturated cotton wool pledglet was then compared. Schmallenberg virus susceptibility was defined by RT-qPCR of RNA extractions of head homogenates and related to Culicoides species and haplotype identifications based on the DNA barcode region of the mitochondrial cytochrome c oxidase 1 (cox1) gene.

Results: Culicoides blood-feeding rates were low across all membrane types tested (7.5% chick skin, 0.0% for collagen, 4.4% Parafilm M®, with 6029 female Culicoides being offered a blood meal in total). Susceptibility to infection with SBV through membrane blood-feeding (8 of 109 individuals tested) and pledglet blood-feeding (1 of 94 individuals tested) was demonstrated for the Obsoletus complex, with both C. obsoletus (Meigen) and C. scoticus Downes & Kettle susceptible to infection with SBV through oral feeding. Potential evidence of cryptic species within UK populations was found for the Obsoletus complex in phylogenetic analyses of cox1 DNA barcodes of 74 individuals assessed from a single field-site.

Conclusions: Methods described in this study provide the means to blood-feed Palaearctic Culicoides for vector competence studies and colonisation attempts. Susceptibility to SBV infection was 7.3% for membrane-fed members of the subgenus Avaritia and 1.1% for pledglet-fed. Both C. obsoletus and C. scoticus were confirmed as being susceptible to infection with SBV, with potential evidence of cryptic species within UK Obsoletus complex specimens, however the implications of cryptic diversity in the Obsoletus complex on arbovirus transmission remains unknown.
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http://dx.doi.org/10.1186/s13071-018-2650-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6389053PMC
February 2018

The Role of Culex pipiens L. (Diptera: Culicidae) in Virus Transmission in Europe.

Int J Environ Res Public Health 2018 02 23;15(2). Epub 2018 Feb 23.

Animal and Plant Health Agency, Woodham Lane, Addlestone, Surrey KT15 3NB, UK.

Over the past three decades, a range of mosquito-borne viruses that threaten public and veterinary health have emerged or re-emerged in Europe. Mosquito surveillance activities have highlighted the species complex as being critical for the maintenance of a number of these viruses. This species complex contains morphologically similar forms that exhibit variation in phenotypes that can influence the probability of virus transmission. Critical amongst these is the choice of host on which to feed, with different forms showing different feeding preferences. This influences the ability of the mosquito to vector viruses and facilitate transmission of viruses to humans and domestic animals. Biases towards blood-feeding on avian or mammalian hosts have been demonstrated for different ecoforms and emerging evidence of hybrid populations across Europe adds another level of complexity to virus transmission. A range of molecular methods based on DNA have been developed to enable discrimination between morphologically indistinguishable forms, although this remains an active area of research. This review provides a comprehensive overview of developments in the understanding of the ecology, behaviour and genetics of in Europe, and how this influences arbovirus transmission.
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http://dx.doi.org/10.3390/ijerph15020389DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5858458PMC
February 2018

Quantification of within- and between-farm dispersal of biting midges using an immunomarking technique.

J Appl Ecol 2017 10 28;54(5):1429-1439. Epub 2017 Feb 28.

The Pirbright Institute Ash Road Pirbright Surrey GU24 0NF UK.

biting midges (Diptera, Ceratopogonidae) are vectors of arboviruses that cause significant economic and welfare impact. Local-scale spread of -borne arboviruses is largely determined by the between-farm movement of infected .Study of the dispersal behaviour of by capture-mark-recapture (CMR) is problematic due to the likelihood of mortality and changes in behaviour upon capture caused by the small size and fragility of these insects, evidenced by low recapture rates. To counter the problem of using CMR with , this study utilised an ovalbumin immunomarking technique to quantify the within- and between-farm dispersal of in southern England.Both within- and between-farm dispersal of was observed. Of the 9058 collected over 22 nights of trapping, 600 ovalbumin-positive , of 12 species including those implicated as arbovirus vectors, were collected with a maximum dispersal distance of 3125 m.This study provides the first species-level data on the between-farm dispersal of potential bluetongue, Schmallenberg and African horse sickness virus vectors in northern Europe. High-resolution meteorological data determined upwind and downwind flight by had occurred. Cumulative collection and meteorological data suggest 15·6% of flights over 1 km were upwind of the treatment area and 84·4% downwind. . The use of immunomarking eliminates the potential adverse effects on survival and behaviour of insect collection prior to marking, substantially improving the resolution and accuracy of estimates of the dispersal potential of small and delicate vector species such as . Using this technique, quantification of the range of dispersal with regard to meteorological conditions including wind direction will enable improved, data-driven modelling of the spread of borne arboviruses and will inform policy response to incursions and outbreaks.
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http://dx.doi.org/10.1111/1365-2664.12875DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5655569PMC
October 2017

How often do mosquitoes bite humans in southern England? A standardised summer trial at four sites reveals spatial, temporal and site-related variation in biting rates.

Parasit Vectors 2017 Sep 15;10(1):420. Epub 2017 Sep 15.

The Pirbright Institute, Ash Road, Woking, Surrey, UK.

Background: This field-based study examined the abundance and species complement of mosquitoes (Diptera: Culicidae) attracted to humans at four sites in the United Kingdom (UK). The study used a systematic approach to directly measure feeding by mosquitoes on humans at multiple sites and using multiple volunteers. Quantifying how frequently humans are bitten in the field by mosquitoes is a fundamental parameter in assessing arthropod-borne virus transmission.

Methods: Human landing catches were conducted using a standardised protocol by multiple volunteers at four rural sites between July and August 2013. Collections commenced two hours prior to sunset and lasted for a total of four hours. To reduce bias occurring due to collection point or to the individual attractiveness of the volunteer to mosquitoes, each collection was divided into eight collection periods, with volunteers rotated by randomised Latin square design between four sampling points per site. While the aim was to collect mosquitoes prior to feeding, the source of blood meals from any engorged specimens was also identified by DNA barcoding.

Results: Three of the four sites yielded human-biting mosquito populations for a total of 915 mosquitoes of fifteen species/species groups. Mosquito species composition and biting rates differed significantly between sites, with individual volunteers collecting between 0 and 89 mosquitoes (over 200 per hour) of up to six species per collection period. Coquillettidia richiardii (Ficalbi, 1889) was responsible for the highest recorded biting rates at any one site, reaching 161 bites per hour, whilst maximum biting rates of 55 bites per hour were recorded for Culex modestus (Ficalbi, 1889). Human-biting by Culex pipiens (L., 1758) form pipiens was also observed at two sites, but at much lower rates when compared to other species.

Conclusions: Several mosquito species are responsible for human nuisance biting pressure in southern England, although human exposure to biting may be largely limited to evening outdoor activities. This study indicates Cx. modestus can be a major human-biting species in the UK whilst Cx. pipiens f. pipiens may show greater opportunistic human-biting than indicated by earlier studies.
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http://dx.doi.org/10.1186/s13071-017-2360-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5602952PMC
September 2017

Insecticidal effects of deltamethrin in laboratory and field populations of Culicoides species: how effective are host-contact reduction methods in India?

Parasit Vectors 2017 01 31;10(1):54. Epub 2017 Jan 31.

Department of Disease Control, Faculty of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, Keppel Street, London, WC1E 7HT, UK.

Background: Bluetongue virus (BTV) is transmitted by Culicoides biting midges and causes bluetongue (BT), a clinical disease observed primarily in sheep. BT has a detrimental effect on subsistence farmers in India, where hyperendemic outbreaks impact on smallholdings in the southern states of the country. In this study, we establish a reliable method for testing the toxic effects of deltamethrin on Culicoides and then compare deltamethrin with traditional control methods used by farmers in India.

Results: Effects of deltamethrin were initially tested using a colonised strain of Culicoides nubeculosus Meigen and a modified World Health Organisation exposure assay. This method was then applied to field populations of Culicoides spp. in India. The field population of C. oxystoma in India had a greater LC (0.012 ± 0.009%) for deltamethrin than laboratory-reared C.nubeculosus (0.0013 ± 0.0002%). Exposure of C. nubeculosus to deltamethrin at higher ambient temperatures resulted in greater rates of knockdown but a lower mortality rate at 24 h post-exposure. Behavioural assays with C. nubeculosus in WHO tubes provided evidence for contact irritancy and spatial repellence caused by deltamethrin. The field experiments in India, however, provided no evidence for repellent or toxic effects of deltamethrin. Traditional methods such as the application of neem oil and burning of neem leaves also provided no protection.

Conclusions: Our study demonstrates that field-collected Culicoides in India are less susceptible to deltamethrin exposure than laboratory-bred C. nubeculosus and traditional methods of insect control do not provide protection to sheep. These low levels of susceptibility to deltamethrin have not been recorded before in field populations of Culicoides and suggest resistance to synthetic pyrethrioids. Alternative insect control methods, in addition to vaccination, may be needed to protect Indian livestock from BTV transmission.
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http://dx.doi.org/10.1186/s13071-017-1992-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5286563PMC
January 2017

African Horse Sickness Virus: History, Transmission, and Current Status.

Annu Rev Entomol 2017 01;62:343-358

Parasites, Vectors, and Vector-Borne Diseases, Agricultural Research Council-Onderstepoort Veterinary Institute, Onderstepoort 0110, South Africa.

African horse sickness virus (AHSV) is a lethal arbovirus of equids that is transmitted between hosts primarily by biting midges of the genus Culicoides (Diptera: Ceratopogonidae). AHSV affects draft, thoroughbred, and companion horses and donkeys in Africa, Asia, and Europe. In this review, we examine the impact of AHSV critically and discuss entomological studies that have been conducted to improve understanding of its epidemiology and control. The transmission of AHSV remains a major research focus and we critically review studies that have implicated both Culicoides and other blood-feeding arthropods in this process. We explore AHSV both as an epidemic pathogen and within its endemic range as a barrier to development, an area of interest that has been underrepresented in studies of the virus to date. By discussing AHSV transmission in the African republics of South Africa and Senegal, we provide a more balanced view of the virus as a threat to equids in a diverse range of settings, thus leading to a discussion of key areas in which our knowledge of transmission could be improved. The use of entomological data to detect, predict and control AHSV is also examined, including reference to existing studies carried out during unprecedented outbreaks of bluetongue virus in Europe, an arbovirus of wild and domestic ruminants also transmitted by Culicoides.
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http://dx.doi.org/10.1146/annurev-ento-031616-035010DOI Listing
January 2017

Advances in control techniques for Culicoides and future prospects.

Vet Ital 2016 Sep;52(3-4):247-264

Vector-borne Viral Diseases Programme, The Pirbright Institute, Ash Road, Pirbright, Surrey, GU24 0NF, United Kingdom.

In most instances, vaccination is accepted to be the most effective method of preventing Culicoides-borne arbovirus transmission, as it has proven to be successful in large-scale campaigns. Under certain scenarios, however, vaccines require time to be developed and deployed or are not used due to financial, logistical or trade constraints. In the absence of vaccines, animal movement restrictions and techniques to reduce either the number of Culicoides biting livestock or their subsequent survival are the only responses available to prevent or reduce arbovirus transmission and spread. This review evaluates the progress made during the past 10 years in the development of Culicoides control techniques for this purpose and assesses their potential impact in reducing arbovirus transmission. In addition, the future prospects and challenges facing Culicoides control are examined and suggestions are made as to research directions and opportunities.
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http://dx.doi.org/10.12834/VetIt.741.3602.3DOI Listing
September 2016

Progress and knowledge gaps in Culicoides genetics, genomics and population modelling: 2003 to 2014.

Authors:
Simon Carpenter

Vet Ital 2016 Sep;52(3-4):201-211

Vector-borne Disease Programme, The Pirbright Institute, United Kingdom.

In the 10 years, since the last international meeting on Bluetongue virus (BTV) and related Orbiviruses in Sicily, there have been huge advances in explorations of the genetics and genomics of Culicoides, culminating in the imminent release of the rst full genome de novo assembly for the genus. In parallel, mathematical models used to predict Culicoides adult distribution, seasonality, and dispersal have also increased in sophistication, re ecting advances in available computational power and expertise. While these advances have focused upon the outbreaks of BTV in Europe, there is an opportunity to extend these techniques to other regions as part of global studies of the genus. This review takes a selective approach to examining the past decade of research in these areas and provides a personal viewpoint of future directions of research that may prove productive.
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http://dx.doi.org/10.12834/VetIt.686.3360.2DOI Listing
September 2016

DNA barcoding and surveillance sampling strategies for Culicoides biting midges (Diptera: Ceratopogonidae) in southern India.

Parasit Vectors 2016 08 22;9:461. Epub 2016 Aug 22.

Vector-borne Viral Diseases Programme, The Pirbright Institute, Ash Road, Woking, Surrey, GU24 0NF, UK.

Background: Culicoides spp. biting midges transmit bluetongue virus (BTV), the aetiological agent of bluetongue (BT), an economically important disease of ruminants. In southern India, hyperendemic outbreaks of BT exert high cost to subsistence farmers in the region, impacting on sheep production. Effective Culicoides spp. monitoring methods coupled with accurate species identification can accelerate responses for minimising BT outbreaks. Here, we assessed the utility of sampling methods and DNA barcoding for detection and identification of Culicoides spp. in southern India, in order to provide an informed basis for future monitoring of their populations in the region.

Methods: Culicoides spp. collected from Tamil Nadu and Karnataka were used to construct a framework for future morphological identification in surveillance, based on sequence comparison of the DNA barcode region of the mitochondrial cytochrome c oxidase I (COI) gene and achieving quality standards defined by the Barcode of Life initiative. Pairwise catches of Culicoides spp. were compared in diversity and abundance between green (570 nm) and ultraviolet (UV) (390 nm) light emitting diode (LED) suction traps at a single site in Chennai, Tamil Nadu over 20 nights of sampling in November 2013.

Results: DNA barcode sequences of Culicoides spp. were mostly congruent both with existing DNA barcode data from other countries and with morphological identification of major vector species. However, sequence differences symptomatic of cryptic species diversity were present in some groups which require further investigation. While the diversity of species collected by the UV LED Center for Disease Control (CDC) trap did not significantly vary from that collected by the green LED CDC trap, the UV CDC significantly outperformed the green LED CDC trap with regard to the number of Culicoides individuals collected.

Conclusions: Morphological identification of the majority of potential vector species of Culicoides spp. samples within southern India appears relatively robust; however, potential cryptic species diversity was present in some groups requiring further investigation. The UV LED CDC trap is recommended for surveillance of Culicoides in southern India.
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http://dx.doi.org/10.1186/s13071-016-1722-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4994320PMC
August 2016

Range expansion of the Bluetongue vector, Culicoides imicola, in continental France likely due to rare wind-transport events.

Sci Rep 2016 06 6;6:27247. Epub 2016 Jun 6.

Cirad, UMR15 CMAEE, 34398; INRA, UMR1309 CMAEE, 34398 Montpellier, France.

The role of the northward expansion of Culicoides imicola Kieffer in recent and unprecedented outbreaks of Culicoides-borne arboviruses in southern Europe has been a significant point of contention. We combined entomological surveys, movement simulations of air-borne particles, and population genetics to reconstruct the chain of events that led to a newly colonized French area nestled at the northern foot of the Pyrenees. Simulating the movement of air-borne particles evidenced frequent wind-transport events allowing, within at most 36 hours, the immigration of midges from north-eastern Spain and Balearic Islands, and, as rare events, their immigration from Corsica. Completing the puzzle, population genetic analyses discriminated Corsica as the origin of the new population and identified two successive colonization events within west-Mediterranean basin. Our findings are of considerable importance when trying to understand the invasion of new territories by expanding species.
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http://dx.doi.org/10.1038/srep27247DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4893744PMC
June 2016

Using shared needles for subcutaneous inoculation can transmit bluetongue virus mechanically between ruminant hosts.

Sci Rep 2016 Feb 8;6:20627. Epub 2016 Feb 8.

The Pirbright Institute, Woking, Surrey, United Kingdom.

Bluetongue virus (BTV) is an economically important arbovirus of ruminants that is transmitted by Culicoides spp. biting midges. BTV infection of ruminants results in a high viraemia, suggesting that repeated sharing of needles between animals could result in its iatrogenic transmission. Studies defining the risk of iatrogenic transmission of blood-borne pathogens by less invasive routes, such as subcutaneous or intradermal inoculations are rare, even though the sharing of needles is common practice for these inoculation routes in the veterinary sector. Here we demonstrate that BTV can be transmitted by needle sharing during subcutaneous inoculation, despite the absence of visible blood contamination of the needles. The incubation period, measured from sharing of needles, to detection of BTV in the recipient sheep or cattle, was substantially longer than has previously been reported after experimental infection of ruminants by either direct inoculation of virus, or through blood feeding by infected Culicoides. Although such mechanical transmission is most likely rare under field condition, these results are likely to influence future advice given in relation to sharing needles during veterinary vaccination campaigns and will also be of interest for the public health sector considering the risk of pathogen transmission during subcutaneous inoculations with re-used needles.
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http://dx.doi.org/10.1038/srep20627DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4745043PMC
February 2016

Can insecticide-treated netting provide protection for Equids from Culicoides biting midges in the United Kingdom?

Parasit Vectors 2015 Nov 25;8:604. Epub 2015 Nov 25.

Vector-borne Viral Diseases Programme, The Pirbright Institute, Ash Road, Pirbright, Surrey, GU24 0NF, UK.

Background: Biting midges of the genus Culicoides Latreille, 1809 (Diptera: Ceratopogonidae) cause a significant biting nuisance to equines and are responsible for the biological transmission of African horse sickness virus (AHSV). While currently restricted in distribution to sub-Saharan Africa, AHSV has a history of emergence into southern Europe and causes one of the most lethal diseases of horses and other species of Equidae. In the event of an outbreak of AHSV, the use of insecticide treated nets (ITNs) to screen equine accomodation is recommended by competent authorities including the Office International des Épizooties (OIE) in order to reduce vector-host contact.

Methods: Seven commercially avaliable pyrethroid insecticides and three repellent compounds, all of which are licensed for amateur use, were assessed in modified World Health Organization (WHO) cone bioassay trials in the laboratory using a colony line of Culicoides nubeculosus (Meigen), 1830. Two field trials were subsequently conducted to test the efficiency of treated net screens in preventing entry of Culicoides.

Results: A formulation of cypermethrin (0.15 % w/w) and pyrethrins (0.2 % w/w) (Tri-Tec 14®, LS Sales (Farnham) Ltd, Bloxham, UK) applied to black polyvinyl-coated polyester insect screen (1.6 mm aperture; 1.6 mm thickness) inflicted 100 % mortality on batches of C. nubeculosus following a three minute exposure in the WHO cone bioassays at 1, 7 and 14 days post-treatment. Tri-Tec 14® outperformed all other treatments tested and was subsequently selected for use in field trials. The first trial demonstrated that treated screens placed around an ultraviolet light-suction trap entirely prevented Culicoides being collected, despite their collection in identical traps with untreated screening or no screening. The second field trial examined entry of Culicoides into stables containing horses and found that while the insecticide treated screens reduced entry substantially, there was still a small risk of exposure to biting.

Conclusions: Screened stables can be utilised as part of an integrated control program in the event of an AHSV outbreak in order to reduce vector-host contact and may also be applicable to protection of horses from Culicoides during transport.
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http://dx.doi.org/10.1186/s13071-015-1182-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4660720PMC
November 2015

Hyaluronidase Activity in Saliva of European Culicoides (Diptera: Ceratopogonidae).

J Med Entomol 2016 Jan 19;53(1):212-6. Epub 2015 Oct 19.

Department of Parasitology, Charles University in Prague, Faculty of Science, Czech Republic

Biting midges of the genus Culicoides transmit pathogens of veterinary importance such as bluetongue virus (Reoviridae: Orbivirus). The saliva of Culicoides is known to contain bioactive molecules including peptides and proteins with vasodilatory and immunomodulative properties. In this study, we detected activity of enzyme hyaluronidase in six Culicoides species that commonly occur in Europe and that are putative vectors of arboviruses. Hyaluronidase was present in all species studied, although its molecular size, sensitivity to SDS, and substrate specificity differed between species. Further studies on the potential effect of hyaluronidase activity on the vector competence of Culicoides species for arboviruses would be beneficial.
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http://dx.doi.org/10.1093/jme/tjv147DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4710844PMC
January 2016

The Biting Midge Culicoides sonorensis (Diptera: Ceratopogonidae) Is Capable of Developing Late Stage Infections of Leishmania enriettii.

PLoS Negl Trop Dis 2015 14;9(9):e0004060. Epub 2015 Sep 14.

Department of Parasitology, Faculty of Science, Charles University, Prague, Czech Republic.

Background: Despite their importance in animal and human health, the epidemiology of species of the Leishmania enriettii complex remains poorly understood, including the identity of their biological vectors. Biting midges of the genus Forcipomyia (Lasiohelea) have been implicated in the transmission of a member of the L. enriettii complex in Australia, but the far larger and more widespread genus Culicoides has not been investigated for the potential to include vectors to date.

Methodology/principal Findings: Females from colonies of the midges Culicoides nubeculosus Meigen and C. sonorensis Wirth & Jones and the sand fly Lutzomyia longipalpis Lutz & Nevia (Diptera: Psychodidae) were experimentally infected with two different species of Leishmania, originating from Australia (Leishmania sp. AM-2004) and Brazil (Leishmania enriettii). In addition, the infectivity of L. enriettii infections generated in guinea pigs and golden hamsters for Lu. longipalpis and C. sonorensis was tested by xenodiagnosis. Development of L. enriettii in Lu. longipalpis was relatively poor compared to other Leishmania species in this permissive vector. Culicoides nubeculosus was not susceptible to infection by parasites from the L. enriettii complex. In contrast, C. sonorensis developed late stage infections with colonization of the thoracic midgut and the stomodeal valve. In hamsters, experimental infection with L. enriettii led only to mild symptoms, while in guinea pigs L. enriettii grew aggressively, producing large, ulcerated, tumour-like lesions. A high proportion of C. sonorensis (up to 80%) feeding on the ears and nose of these guinea pigs became infected.

Conclusions/significance: We demonstrate that L. enriettii can develop late stage infections in the biting midge Culicoides sonorensis. This midge was found to be susceptible to L. enriettii to a similar degree as Lutzomyia longipalpis, the vector of Leishmania infantum in South America. Our results support the hypothesis that some biting midges could be natural vectors of the L. enriettii complex because of their vector competence, although not Culicoides sonorensis itself, which is not sympatric, and midges should be assessed in the field while searching for vectors of related Leishmania species including L. martiniquensis and "L. siamensis".
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http://dx.doi.org/10.1371/journal.pntd.0004060DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4569557PMC
March 2016