Lack of Vector Competence in UK Culex pipiens molestus for Oropouche Virus

Lack of Vector Competence in UK Culex pipiens molestus for Oropouche Virus | bioRxiv /* */ /* */ <!-- <!-- /*! * yepnope1.5.4 * (c) WTFPL, GPLv2 */ (function(a,b,c){function d(a){return"[object Function]"==o.call(a)}function e(a){return"string"==typeof a}function f(){}function g(a){return!a||"loaded"==a||"complete"==a||"uninitialized"==a}function h(){var a=p.shift();q=1,a?a.t?m(function(){("c"==a.t?B.injectCss:B.injectJs)(a.s,0,a.a,a.x,a.e,1)},0):(a(),h()):q=0}function i(a,c,d,e,f,i,j){function k(b){if(!o&&g(l.readyState)&&(u.r=o=1,!q&&h(),l.onload=l.onreadystatechange=null,b)){"img"!=a&&m(function(){t.removeChild(l)},50);for(var d in y[c])y[c].hasOwnProperty(d)&&y[c][d].onload()}}var j=j||B.errorTimeout,l=b.createElement(a),o=0,r=0,u={t:d,s:c,e:f,a:i,x:j};1===y[c]&&(r=1,y[c]=[]),"object"==a?l.data=c:(l.src=c,l.type=a),l.width=l.height="0",l.onerror=l.onload=l.onreadystatechange=function(){k.call(this,r)},p.splice(e,0,u),"img"!=a&&(r||2===y[c]?(t.insertBefore(l,s?null:n),m(k,j)):y[c].push(l))}function j(a,b,c,d,f){return q=0,b=b||"j",e(a)?i("c"==b?v:u,a,b,this.i++,c,d,f):(p.splice(this.i++,0,a),1==p.length&&h()),this}function k(){var a=B;return a.loader={load:j,i:0},a}var l=b.documentElement,m=a.setTimeout,n=b.getElementsByTagName("script")[0],o={}.toString,p=[],q=0,r="MozAppearance"in l.style,s=r&&!!b.createRange().compareNode,t=s?l:n.parentNode,l=a.opera&&"[object Opera]"==o.call(a.opera),l=!!b.attachEvent&&!l,u=r?"object":l?"script":"img",v=l?"script":u,w=Array.isArray||function(a){return"[object Array]"==o.call(a)},x=[],y={},z={timeout:function(a,b){return b.length&&(a.timeout=b[0]),a}},A,B;B=function(a){function b(a){var a=a.split("!"),b=x.length,c=a.pop(),d=a.length,c={url:c,origUrl:c,prefixes:a},e,f,g;for(f=0;f<d;f++)g=a[f].split("="),(e=z[g.shift()])&&(c=e(c,g));for(f=0;f<b;f++)c=x[f](c);return c}function g(a,e,f,g,h){var i=b(a),j=i.autoCallback;i.url.split(".").pop().split("?").shift(),i.bypass||(e&&(e=d(e)?e:e[a]||e[g]||e[a.split("/").pop().split("?")[0]]),i.instead?i.instead(a,e,f,g,h):(y[i.url]?i.noexec=!0:y[i.url]=1,f.load(i.url,i.forceCSS||!i.forceJS&&"css"==i.url.split(".").pop().split("?").shift()?"c":c,i.noexec,i.attrs,i.timeout),(d(e)||d(j))&&f.load(function(){k(),e&&e(i.origUrl,h,g),j&&j(i.origUrl,h,g),y[i.url]=2})))}function h(a,b){function c(a,c){if(a){if(e(a))c||(j=function(){var a=[].slice.call(arguments);k.apply(this,a),l()}),g(a,j,b,0,h);else if(Object(a)===a)for(n in m=function(){var b=0,c;for(c in a)a.hasOwnProperty(c)&&b++;return b}(),a)a.hasOwnProperty(n)&&(!c&&!--m&&(d(j)?j=function(){var a=[].slice.call(arguments);k.apply(this,a),l()}:j[n]=function(a){return function(){var b=[].slice.call(arguments);a&&a.apply(this,b),l()}}(k[n])),g(a[n],j,b,n,h))}else!c&&l()}var h=!!a.test,i=a.load||a.both,j=a.callback||f,k=j,l=a.complete||f,m,n;c(h?a.yep:a.nope,!!i),i&&c(i)}var i,j,l=this.yepnope.loader;if(e(a))g(a,0,l,0);else if(w(a))for(i=0;i (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0];var j=d.createElement(s);var dl=l!='dataLayer'?'&l='+l:'';j.src='//www.googletagmanager.com/gtm.js?id='+i+dl;j.type='text/javascript';j.async=true;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-M677548'); Skip to main content Home About Submit ALERTS / RSS Search for this keyword Advanced Search New Results Lack of Vector Competence in UK Culex pipiens molestus for Oropouche Virus View ORCID Profile Jack Pilgrim , Victoria E Sy , Quentin Multeau , View ORCID Profile Thamil Vaani Komarasamy , View ORCID Profile Alain Kohl , View ORCID Profile Marcus SC Blagrove , View ORCID Profile Jolanta Tanianis-Hughes , View ORCID Profile Jolyon Medlock , View ORCID Profile Christopher Sanders , View ORCID Profile Matthew Baylis , View ORCID Profile Isabelle Dietrich doi: https://doi.org/10.1101/2025.05.07.652619 Jack Pilgrim 1 Institute of Infection, Veterinary and Ecological Sciences, Faculty of Health and Life Sciences, University of Liverpool , Liverpool, L69 3BX, UK Find this author on Google Scholar Find this author on PubMed Search for this author on this site ORCID record for Jack Pilgrim Victoria E Sy 2 The Pirbright Institute , Ash Road, Pirbright GU24 0NF, UK Find this author on Google Scholar Find this author on PubMed Search for this author on this site Quentin Multeau 2 The Pirbright Institute , Ash Road, Pirbright GU24 0NF, UK Find this author on Google Scholar Find this author on PubMed Search for this author on this site Thamil Vaani Komarasamy 2 The Pirbright Institute , Ash Road, Pirbright GU24 0NF, UK Find this author on Google Scholar Find this author on PubMed Search for this author on this site ORCID record for Thamil Vaani Komarasamy Alain Kohl 3 Centre for Neglected Tropical Diseases, Departments of Tropical Disease Biology and Vector Biology, Liverpool School of Tropical Medicine , Liverpool, L3 5QA, UK Find this author on Google Scholar Find this author on PubMed Search for this author on this site ORCID record for Alain Kohl Marcus SC Blagrove 1 Institute of Infection, Veterinary and Ecological Sciences, Faculty of Health and Life Sciences, University of Liverpool , Liverpool, L69 3BX, UK Find this author on Google Scholar Find this author on PubMed Search for this author on this site ORCID record for Marcus SC Blagrove Jolanta Tanianis-Hughes 1 Institute of Infection, Veterinary and Ecological Sciences, Faculty of Health and Life Sciences, University of Liverpool , Liverpool, L69 3BX, UK Find this author on Google Scholar Find this author on PubMed Search for this author on this site ORCID record for Jolanta Tanianis-Hughes Jolyon Medlock 4 Medical Entomology and Zoonoses Ecology group, UK Health Security Agency , Porton Down, Salisbury SP4 0JG, UK Find this author on Google Scholar Find this author on PubMed Search for this author on this site ORCID record for Jolyon Medlock Christopher Sanders 2 The Pirbright Institute , Ash Road, Pirbright GU24 0NF, UK Find this author on Google Scholar Find this author on PubMed Search for this author on this site ORCID record for Christopher Sanders Matthew Baylis 1 Institute of Infection, Veterinary and Ecological Sciences, Faculty of Health and Life Sciences, University of Liverpool , Liverpool, L69 3BX, UK Find this author on Google Scholar Find this author on PubMed Search for this author on this site ORCID record for Matthew Baylis Isabelle Dietrich 2 The Pirbright Institute , Ash Road, Pirbright GU24 0NF, UK Find this author on Google Scholar Find this author on PubMed Search for this author on this site ORCID record for Isabelle Dietrich For correspondence: Isabelle.Dietrich{at}pirbright.ac.uk Abstract Full Text Info/History Metrics Supplementary material Preview PDF Abstract Oropouche virus (OROV) is an orthobunyavirus ( Peribunyaviridae ) that has caused recurrent outbreaks in South America and has recently expanded into the Caribbean, with various biting midge and mosquito species considered vectors. Recent imported cases to Europe and North America have raised concerns about the potential for local transmission in non-endemic areas. To assess this risk in the United Kingdom, we investigated the vector competence of Culex pipiens molestus ( Cx. molestus ), a human-biting mosquito common in urban environments. Laboratory-reared adult females were fed a bloodmeal containing a Cuban 2024 OROV outbreak strain (240023) and maintained at 27°C. Of 64 individuals tested at 12-s14 days post-infection via plaque assay, none were positive for OROV in bodies, indicating no evidence of infection and subsequently limited or no vector competence potential. These results provide evidence that UK populations of Cx. molestus are unlikely to support OROV transmission, thereby refining assessments of OROV emergence risk in temperate settings. Further studies are needed to test other putative UK mosquito vectors, as well as Culicoides biting midge species to fully assess the potential for OROV transmission in this region. Introduction Oropouche virus (OROV) is an emerging orthobunyavirus ( Peribunyaviridae ) endemic to South America which has, periodically, caused epidemics in people living in the Amazon region. Since 2023, the largest outbreak on record has affected several countries in South America [ 1 , 2 ] and has also spread for the first time to Cuba [ 3 ], thus expanding its geographical range. Travellers, mostly from Cuba, have brought OROV to North America [ 4 ] and Europe [ 5 ], raising the risk of its spread and emergence to new areas. OROV is transmitted in South America primarily by a species of Ceratopogonid biting midge, Culicoides paraensis [ 6 ], which is a diurnally active species that readily feeds on humans in urban settings. Other species of human-feeding biting midges may also be implicated (for example, C. furens and C. insignis ), as are several species of mosquito, most notably the very widespread species in tropical climates Culex quinquefasciatus , which has frequently been found positive for OROV in the field and shown to be susceptible in the laboratory [ 7 , 8 ]. However, studies have shown that Cx. quinquefasciatus is not consistently competent following oral infection, indicating that evidence for Culex spp. as a vector is likely context-dependent [ 9 ]. Notably, recent genomic analyses suggest that the virus involved in the current outbreak is a reassortant [ 10 ], potentially exhibiting altered pathogenicity and an expanded range of competent vector species. The introduction of OROV into other parts of the world by travellers from South America and the Caribbean raises the general question of whether midges and mosquitoes found in those regions are competent to transmit the virus to humans. Here, we consider the specific question of whether UK mosquitoes are competent to transmit OROV. Cx. quinquefasciatus is absent from the UK but it is a member of the Cx. pipiens assemblage, which includes the species Cx. pipiens sensu strictu. Cx. pipiens is found throughout the UK, often in close proximity to people. It occurs in the UK in three biotypes: the bird-biting Cx. pipiens pipiens , the human-biting Cx. pipiens molestus (hereafter Cx. molestus ), and hybrids between the two [ 11 ]. All three biotypes feed on humans to differing extents and hence could present a public health threat from OROV. The highest risk vector is most likely Cx. molestus , which, where it is locally abundant [ 12 ], could feed on a traveller, become infected and transmit the infection to other people. Here we investigated the competence of a colony of Cx. molestus established from collections in Surrey, southeast England, UK, for OROV. This was achieved by feeding adult females a virus-spiked bloodmeal, maintaining them at constant temperature and then, after several days, testing their bodies, legs and wings, and saliva for OROV by plaque assay as a measure of virus infection, dissemination and transmission, respectively. Materials and methods Mosquito maintenance The Cx. molestus colony was derived from a mixed field population of Cx. pipiens s.l. (“Brookwood”) collected in 2011 from Surrey, UK [ 13 ]. Briefly, Cx. molestus were bred by rearing egg rafts from the mixed population, identifying emerging adults by biotype using molecular markers from pupal exuviae, and subsequently maintaining individual Cx. molestus biotypes through subsequent generations [ 14 ]. Egg rafts were hatched in 35 × 25 × 5 cm larval trays with 2 litres of tap water. Larvae were provided with 125 mg Brewer’s Yeast (Holland’s and Barrett, UK) added every 2 days until pupation. Adults then emerged in 30 × 30 × 30 cm BugDorm cages (BugDorm, Taichung, Taiwan) and were maintained at 27°C and 60% relative humidity in a 12:12 inverted light:dark cycle with 10 % sucrose solution and water until infection experiments. Virus The 240023 strain of OROV, originally isolated from a febrile patient from Cuba [ 15 ] was kindly provided by the World Reference Centre for Emerging Viruses and Arboviruses (WRCEVA) at the University of Texas Medical Branch at Galveston, Texas, USA. Virus was passaged once on Vero cells (ATCC, Manassas, VA, USA) at low MOI for 5 days at 33°C and 5% CO2. To increase viral stock titres for mosquito infections, virus was concentrated over Amicon 100 kDa MW 15 ml columns (Merck, Feltham, UK). Virus stocks were titrated by plaque assay on Vero cells. Cells were incubated for 3 days at 37°C and 5% CO2 using Minimal Essential Medium (MEM; Fisher Scientific, Loughborough, UK) supplemented with 2% foetal calf serum (FCS; Fisher Scientific) and 0.6% Avicel (FMC Corporation/Roquette, London, UK) as overlay, fixed using 4% formaldehyde and stained using 0.1% (w/v) toluidine blue. All infection work was undertaken in specialised, licensed category 3 containment laboratories at The Pirbright Institute by trained personnel. Mosquito infection studies Prior to infection, 9-20 day old female mosquitoes were starved of sucrose and water for 16 hours. They were cold-anesthetised and sorted into 4 oz espresso cups covered by fine mesh. On the day of infection, an infectious blood meal was prepared containing two-thirds defibrinated horse blood (TCS Biosciences, Buckingham, UK), one third virus at a final titre of 6.5 log10 PFU/ml and dATP (Thermo Fisher Scientific, Hemel Hempstead, UK) as a phagostimulant at a final concentration of 5 mM. Mosquitoes were fed using a Hemotek feeding system (Hemotek, Blackburn, UK) set up at 36-37°C. Reservoirs were covered with one layer of hog gut and one layer of parafilm, and blood was offered to mosquitoes for 1-2 hours in a class III microbiological safety cabinet in the dark. Mosquitoes were cold-anesthetised and engorged individuals sorted into fresh cups. Non-fed females were discarded. Mosquitoes were maintained for 12-14 days at 27°C. 10% sucrose solution on cotton was provided throughout as source of nutrition and water. Mosquito sampling On days 12-14 post blood-meal, mosquitoes were cold-anesthetised, legs and wings removed and stored in 200 μl virus isolation media (VIM). VIM consisted of Dulbecco’s Modified Eagle Medium (DMEM) supplemented with 2% FCS, 100 I.U./ml penicillin, 100 μg/ml streptomycin, 50 μg/ml gentamycin and 2.5 μg/ml amphotericin B (all Fisher Scientific). Saliva was collected via the capillary method using 200 μl pipette tips containing 20 μl of 50% sucrose (w/v) (Fisher Scientific)– FCS (1:1) for 30-60 minutes. Saliva was combined with 180 μl VIM. Bodies were then collected in separate tubes containing 200 μl VIM. Body, leg and wing sample tubes contained a 2.5 mm sterile stainless steel ball bearing (Dejay Distribution, Launceston, UK). Samples were stored at -80°C until further use. Testing of mosquitoes for OROV Body samples were homogenised at 25 Hz for 2 × 40 seconds using a Tissuelyser II system (Qiagen, Manchester, UK). Homogenate was clarified by centrifugation at 10,000 xg for 5 minutes at 4°C and supernatant was used for serial titration. Viral titres were quantified by plaque assay as described above to determine infectivity in bodies. As no bodies positive for virus infection were found, leg and wing and saliva samples were not titrated in this study. Results None of the mosquito bodies tested positive for OROV by titration ( Table 1 ). The absence of OROV infection in mosquito bodies suggests that the virus is not competent to establish midgut infections in this species. As a result, further testing for viral dissemination or transmission via saliva or legs/wings was unnecessary for these individuals. Using the Clopper–Pearson Exact method, the upper bounds of the 95% and 99% confidence intervals for the true infection rate were estimated to be 5.60% and 7.95%, respectively. View this table: View inline View popup Download powerpoint Table 1. Infection outcomes in Culex pipiens molestus following oral exposure to OROV strain 240023. N/A = Not Applicable. Discussion Our results could not find any evidence for vector competence of UK Cx. molestus for OROV, an outcome that is reassuring as Cx. molestus is a voracious human feeder that is closely related to a known vector, Cx. quinquefasciatus. Cx. molestus has a very focal distribution, mostly found underground and occasionally above ground [ 12 ]. Far more widespread and common in the UK is the Cx. pipiens biotype which is found throughout the country in both rural and urban environments [ 16 ]. It often breeds in rain harvesters or other water containers in gardens; it is probably the mosquito most frequently encountered by people and it will occasionally feed on them. However, while Cx. molestus is primarily a human feeder, Cx. pipiens is primarily a bird feeder. Recent assessment of vector competency for OROV of Cx. pipiens from the USA demonstrated one saliva positive out of 50 tested for the same virus used in this study (240023) suggesting that although transmission is possible, risk remains very low [ 15 ]. Given the close relatedness of Cx. molestus and Cx. pipiens , this suggests that vector competence for OROV across the species complex is likely to be minimal. After feeding, the Cx. molestus in our study were maintained at 27°C until harvesting, mimicking achievable summer temperatures in England. Many mosquito-virus systems show increased infection and transmission rates at higher temperatures, despite local cooler environmental conditions [ 17 , 18 ]. However, this is not universally observed, with UK-derived Cx. pipiens showing high competence for the flavivirus Japanese encephalitis virus (JEV) when maintained at 18°C [ 19 ], suggesting that cold-adapted mosquitoes may, in some cases, be more susceptible at lower temperatures [ 20 ]. It is therefore important to follow up our initial experiments with studies at lower temperatures. Similarly, there are several other UK species of mosquito that feed readily on people; for example, Aedes vexans and the salt marsh mosquito, Ochlerotatus (Aedes) detritus . The latter species has been shown to be competent to transmit several flaviviruses and alphaviruses (JEV, West Nile virus, Zika virus, Ross River virus) [ 19 – 22 ] and transmit the bunyavirus Rift Valley fever virus [ 23 ], while attempts to infect with dengue virus (a flavivirus) and chikungunya virus (an alphavirus) were unsuccessful [ 20 ]. Given its demonstrated competence for some arboviruses, investigation of the competence of Och. detritus for OROV should be prioritised. A greater risk to people in the UK may arise from Culicoides biting midges which are diverse and widespread. The majority of species feed primarily on animals but some more generalist feeders are known to feed occasionally on people. This includes the widespread C. obsoletus species group and the Scottish biting midge, C. impunctatus , which reaches extremely high abundances in suitable habitats in the UK, especially the West of Scotland [ 24 ]. C. impunctatus is autogenous (meaning that mated females can lay their first egg batch without having taken a bloodmeal) and these high abundances can therefore be achieved where there are few or no suitable hosts. Consequently, the vast majority of adult C. impunctatus probably never take a bloodmeal. As transmission of OROV in the UK would require a vector to feed at least twice on humans (as there are no known reservoir species), in sparsely populated areas like Western Scotland it seems inherently unlikely that any C. impunctatus would achieve this, although there may be certain areas frequented by people where the probability of sequential human feeds is higher. Overall, the capacity of C. impunctatus to spread OROV is likely to be low, even if it is competent. Some Culicoides species (e.g., C. obsoletus, C. pulicaris, C. punctatus ) can be a biting nuisance in peri-domestic environments [ 25 ] and investigation of their competence for OROV should be prioritised. Author contributions JM, MB, MSCB, AK, CS and ID secured funding for this project. ID, MB, MSCB, JM, JP, CS and VES contributed to the conceptual development of the project. JP, JTH and QM maintained mosquitoes and prepared adults for infection experiments. ID and TVK prepared virus stocks and performed virus titrations. ID and VS conducted mosquito infection work. ID, MB and JP interpreted data and produced the first draft of the manuscript. All authors assisted in critical revision of the manuscript. Funding This research was funded by a HPRU-EZI award to JM, MB, MSCB, JP, AK, CS and ID. Research conducted at The Pirbright Institute was further supported by funding from the Biotechnology and Biological Sciences Research Council (BBS/E/PI/230002C, BBS/E/PI/23NB0004, BBS/E/PI/23NB0003). Conflicts of interest The authors declare that there are no conflicts of interest. 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Share Lack of Vector Competence in UK Culex pipiens molestus for Oropouche Virus Jack Pilgrim , Victoria E Sy , Quentin Multeau , Thamil Vaani Komarasamy , Alain Kohl , Marcus SC Blagrove , Jolanta Tanianis-Hughes , Jolyon Medlock , Christopher Sanders , Matthew Baylis , Isabelle Dietrich bioRxiv 2025.05.07.652619; doi: https://doi.org/10.1101/2025.05.07.652619 Share This Article: Copy Citation Tools Lack of Vector Competence in UK Culex pipiens molestus for Oropouche Virus Jack Pilgrim , Victoria E Sy , Quentin Multeau , Thamil Vaani Komarasamy , Alain Kohl , Marcus SC Blagrove , Jolanta Tanianis-Hughes , Jolyon Medlock , Christopher Sanders , Matthew Baylis , Isabelle Dietrich bioRxiv 2025.05.07.652619; doi: https://doi.org/10.1101/2025.05.07.652619 Citation Manager Formats BibTeX Bookends EasyBib EndNote (tagged) EndNote 8 (xml) Medlars Mendeley Papers RefWorks Tagged Ref Manager RIS Zotero Tweet Widget Facebook Like Google Plus One Subject Area Microbiology Subject Areas All Articles Animal Behavior and Cognition (7616) Biochemistry (17625) Bioengineering (13852) Bioinformatics (41825) Biophysics (21397) Cancer Biology (18524) Cell Biology (25417) Clinical Trials (138) Developmental Biology (13350) Ecology (19858) Epidemiology (2067) Evolutionary Biology (24277) Genetics (15581) Genomics (22459) Immunology (17698) Microbiology (40278) Molecular Biology (17134) Neuroscience (88400) Paleontology (666) Pathology (2823) Pharmacology and Toxicology (4812) Physiology (7632) Plant Biology (15106) Scientific Communication and Education (2042) Synthetic Biology (4281) Systems Biology (9807) Zoology (2266)