mve12010

Medical and Veterinary Entomology (2013), doi: 10.1111/mve.12010

S H O R T C O M M U N I C A T I O N

No evidence for the persistence of Schmallenberg virusin overwintering mosquitoes

E. J. S C H O L T E 1, M. H. M A R S2, M. B R A K S3, W. D E N H A R T O G 1,A. I B A N E Z - J U S T I C I A1, M. K O O P M A N S4, J. C. M. K O E N R A A D T 5,A. D E V R I E S4 and C. R E U S K E N4

1Dutch National Centre for Monitoring of Vectors (CMV), Netherlands Food and Consumer Product Safety Authority (NVWA),

Wageningen, The Netherlands, 2Animal Health Service (GD), Deventer, The Netherlands, 3Centre for Zoonoses and

Environmental Microbiology, Centre for Infectious Disease Control, National Institute for Public Health and the Environment

(RIVM), Bilthoven, The Netherlands, 4Centre for Infectious Disease Research, Diagnostics and Screening, Centre for Infectious

Disease Control, National Institute for Public Health and the Environment (RIVM), Bilthoven, The Netherlands and 5Laboratory

of Entomology, Wageningen University and Research (WUR), Wageningen, The Netherlands

Abstract. In 2011, Schmallenberg virus (SBV), a novel member of the Simbuserogroup, genus Orthobunyavirus , was identified as the causative agent of a diseasein ruminants in Europe. Based on the current knowledge on arthropods involvedin the transmission of Simbu group viruses, a role of both midges and mosquitoesin the SBV transmission cycle cannot be excluded beforehand. The persistence ofSBV in mosquitoes overwintering at SBV-affected farms in the Netherlands wasinvestigated. No evidence for the presence of SBV in 868 hibernating mosquitoes(Culex , Anopheles , and Culiseta spp., collected from January to March 2012) wasfound. This suggests that mosquitoes do not play an important role, if any, in thepersistence of SBV during the winter months in northwestern Europe.

Key words. Mosquito, overwintering, schmallenberg virus, vector.

In November 2011, a novel orthobunyavirus, named Schmal-lenberg virus (SBV), was identified as the causative agent ofa specific syndrome in ruminants in nine European countries,including the Netherlands. The clinical signs include fever,diarrhoea, milk drop in cattle and typical severe congenitalmalformations owing to transplacental transmission (Hoffmannet al ., 2012; Muskens et al ., 2012). According to estima-tions of the European Food Safety Authority, SBV circulatedin the Netherlands between July and December 2011, withmost intense transmission in August and September (EFSA,2012).

Full genome and serological investigations have identifiedSBV as most related to Sathuperi (SATV) virus and as a possi-ble ancestor of Shamonda virus (SHAV) (Goller et al ., 2012).These viruses belong to the Simbu serogroup of the Orthobun-yavirus genus, family Bunyaviridae. Orthobunyaviruses are

Correspondence: Ernst Jan Scholte, Dutch National Centre for Monitoring of Vectors (CMV), Netherlands Food and Consumer Product SafetyAuthority (NVWA), Wageningen 6700 HC, The Netherlands. Tel.: 0031317496908; E-mail: [email protected]; Chantal Reusken, Centre forInfectious Disease Control, National Institute for Public Health and the Environment (RIVM), PO Box 1, 3720 BA, Bilthoven, The Netherlands.Tel.: 0031302743390; Fax: 0031302744418; E-mail: [email protected]

known to be vector-borne (Yanase et al ., 2012). From the25 viruses belonging to the Simbu serogroup, 14 have beendetected in/isolated from biting midges (Culicoides , Cerato-pogonidae) and 15 from mosquitoes (family Culicidae, variousgenera) (Table 1). Eight Simbu serogroup viruses, includingSATV, have been detected in both types of arthropods. Thedetection of SBV RNA in several Culicoides species (Obso-letus group, C . dewulfi and C . chiopterus) collected in 2011in Belgium, Denmark, the Netherlands, and Italy, especiallywhere the virus was detected in the heads of Culicoides (DeRegge et al ., 2012; Elbers et al ., 2013) implies that SBV isvector-borne as well and that Culicoides are strongly suspectedto play a role in the SBV transmission cycle (De Regge et al .,2012; ProMED-Mail, 2012a, b; Rasmussen et al ., 2012; Elberset al ., 2013). Whether mosquitoes are involved in the SBV lifecycle is not known yet.

© 2013 The Royal Entomological Society 1

2 E. J. Scholte et al.

Table 1. Simbu serogroup viruses, and their known or suspected vectors.

Reported vector∗

Virus Abbr.CulicoidesBiting midge

CulicidaeMosquito

Species (and methodologyused for detection) References

Schmallenberg SMV Yes Unknown Culicoides obsoletus (PCR) andC. dewulfi (PCR)

Rasmussen et al . (2012) andProMED-Mail (2012a)

Shamonda SHA Yes Unknown Culicoides spp., C . imicola , C.pallidipennis ( all threeisolation)

Yanase et al . (2005), Lee(1979), Causey et al . (1972)and Calisher (1996)

Sathuperi SAT Yes Yes Culex vishnui (isolation) andCulicoides spp. (isolation)

Causey et al . (1972), Dandawateet al . (1977), Reuben et al .(1988), Yanase et al . (2004)and Lee (1979)

Akabane AKA Yes Yes Aedes vexans , Anophelesfunestus , Culextritaeniorhynchus (isolation),Culicoides brevitarsis(isolation)

Jennings & Mellor (1989), Oyaet al . (1961) and Metselaar &Robin (1976)

Aino AINO Unknown Yes Culex tritaeniorrhynchus , Culexpipiens/pseudovishnui(isolation)

Saeed et al . (2001) andTakahashi et al . (1968)

Douglas DOU Yes Unknown Culicoides brevitarsis (isolation) Cybinski (1984) and Ward(1995)

Oropouche ORO Yes Yes Coquillettidia venezuelensi ,Aedes Serratus , Culexquinquefasciatus (isolation)and Culicoides paraensis(isolation)

Saeed et al . (2001) and Nuneset al . (2005)

Ingwavuma ING Unknown Yes Culex neavei (isolation) Converse et al . (1985) and Topet al . (1974)

Inini INI Unknown Unknown — no literature foundJatobal JAT Unknown Unknown Isolated only once, from a

carnivoreSaeed et al . (2001)

Kaikalur KAI Unknown Yes Culex tritaeniorhynchus Rodrigues et al . (1977) andReuben et al . (1988)

Manzanilla MAN Unknown Yes Culex fatigans , Aedes serratus ,Aedes scapularis (vectorcompetence study)

Anderson et al . (1960)

Mermet MER Unknown Yes Culex restuans , Culex pipiens(isolation)

Jakob et al . (1979) and Calisheret al . (1981)

Facey’s Paddock FP Unknown Yes Culex annulirostris (isolation) Lee et al . (1989) and Saeedet al . (2001) no

Para PARA Unknown Unknown — literature foundPeaton PEA Yes Unknown Culicoides brevitarsis (isolation) Stgeorge et al . (1980) and

Matsumori et al . (2002)Sabo SABO Yes Unknown Culidoides pallidipennis

(isolation)Lee (1979) and ICTVdB (2004),

Index of virusesSango SAN Yes Yes Culicoides spp. (isolation),

Mansonia uniformis(isolation)

Lee (1979), Metselaar et al .(1974) and ICTVdB (2004),Index of viruses

Buttonwillow BUT Yes Yes Culidoides variipennis(isolation). Culex tarsalis ,Anopheles pseudopunctipennisfranciscanus , Ae. aegypti(vector comp. study)

Reeves et al . (1970) and Hardyet al . (1972)

Shuni SHU Yes Yes Culicoides spp. (isolation) andmosquitoes

Lee (1979), Coetzer & Erasmus(1994) and Causey et al .(1972)

Simbu SIM Unknown Yes Aedes circumluteolus (isolation) McIntosh (1975) and Weinbrenet al . (1957)

© 2013 The Royal Entomological Society, Medical and Veterinary Entomology, doi: 10.1111/mve.12010

No Schmallenberg virus in hibernating mosquitoes 3

Table 1. Continued

Reported vector∗

Virus Abbr.CulicoidesBiting midge

CulicidaeMosquito

Species (and methodologyused for detection) References

Tinaroo TIN Yes Unknown Culicoides brevitarsis (isolation) Cybinski (1984) and Saeed et al .(2001)

Thimiri THI Yes Unknown Culicoides histrio (isolation) Standfast & Dyce (1982) andYanase et al . (2004)

Yaba-7 YABA Unknown Yes Culicidae (isolation) Causey et al . (1972), Hardyet al . (1972) and Saeed et al .(2001)

Utinga UTI Unknown Unknown Isolated only from sloth, notfrom vectors

Mahy (2001) and ICTVdB(2004), Index of viruses

∗Two different vector taxon levels are used in this table. Both biting midges and mosquitoes belong to the order Diptera and suborder Nematocera.‘Biting midges’ belong to the family Ceratopogonidae, which contains several genera, among them Culicoides . Mosquitoes belong to the familyCulicidae, which contains many genera, the most common ones being Culex , Aedes , Anopheles , Culiseta , Coquillettidia and Mansonia .

An important question, relevant for understanding the epi-demiology of a vector-borne disease, is whether vectors canconstitute a vehicle for survival of the virus in periods withminimal vector activity or virus circulation. The mechanismsunderlying arbovirus persistence in arthropods through wintersare not fully understood. In temperate Europe, midges are pre-sumed to overwinter as larvae, making vertical transmissiona prerequisite for virus overwintering in these invertebrates(Wilson & Mellor, 2009; Napp et al ., 2011). On the otherhand, multiple mosquito species are known to overwinter asadults, thereby allowing additional routes of arbovirus winterpersistence: (a) venerally acquired infection; (b) prolonged sur-vival of non-diapausing females in a state of quiescence; (c)pre-hibernation bloodmeals from hibernation-destined (winter-diapause) females and (d) gonotrophic dissociation (blood-meals taken during winter-diapause) (Reeves, 1987, 1990;Reisen, 1990). Examples of virus retrieval from overwinter-ing mosquitoes include West Nile virus (WNV), St. Louisencephalitis (SLEV) and Usutu virus from Culex pipiens (Bai-ley et al ., 1978; Nasci et al ., 2001; ProMED-Mail, 2012c),Western equine encephalitis virus from Cx . tarsalis (Reeveset al ., 1958) and Eastern equine encephalitis from Culisetaspp. (Reisen, 1990).

We investigated the presence of SBV in mosquitoesoverwintering at 11 ruminant farms, where between November2011 and January 2012 SBV circulation had been proven basedon the presence of SBV RNA in the brains of malformednewborns. These farms were located in different regions in theNetherlands (Fig. 1). Hibernating mosquitoes were collectedat their resting places in indoor and outdoor structures using astrong flashlight and a suction tube. Temperatures, as measuredduring the indoor mosquito collections by means of a datalogger, ranged from 2 to 8 ◦C. The indoor structures wereunheated and included barns with ruminants (cattle or sheep),empty barns, hay-stacks, storage barns, lofts, temporarilyunused rooms and sheds, and one cellar. Outdoor structuresincluded hollow trees, a loose-tarpaulin-covered boat and ahalf-open greenhouse. Animal holdings were visited oncefor approximately 3 h each in the period from 12 January

to 8 March 2012. All except three [Cx . pipiens sensu lato(s.l.)] hibernating mosquitoes were collected indoors. Collectedmosquitoes were kept alive during transport, subsequently keptat 4 ◦C for 1–5 days and then killed by placing them at −20 ◦Cfor 15–30 min. For the identification of mosquitoes, standardmorphological keys were used (Schaffner et al ., 2001) 116An . maculipennis s.l. specimens were further diagnosed bymolecular diagnostics (Proft et al ., 1999) up to the siblingspecies level [An . messae, An . atroparvus , or An . maculipennissensu stricto (s.s)]. For all specimens it was registered whethera bloodmeal had been taken or not. Specimens were kept inRNAlater buffer and pooled per species per farm and collectiondate with a maximum of 10 mosquitoes per pool.

The collected adult mosquitoes, all female, belonged tofour species: Anopheles maculipennis s.l. (n = 325), Culisetaannulata (n = 274), Culex pipiens s.l. (n = 1187) and Culexterritans (n = 12). Of the 116 An . maculipennis s.l. that werefurther diagnosed, 102 were An . messae, 14 An . atroparvusand 0 An . maculipennis s.s. The 14 An . atroparvus werefound on three sites in the coastal areas of the Netherlands(Middelburg, Oosterend and Den Burg). An . maculipennisis known to take prehibernation bloodmeals and to exhibitgonotrophic dissociation, both putative routes for acquiringSBV from viremic ruminants (Schwellengrebel, 1928; Reisen,1990). Indeed 20 of the 325 An . maculipennis (6.2%) wereblood-fed, confirming the take of mid-winter bloodmeals. Thisstudy strongly suggests that Cs . annulata exhibits gonotrophicdissociation as well: 128 out of the 274 Cs . annulata (46.7%)were freshly blood-fed. All mosquitoes from these two specieswere tested for the presence of SBV.

Cx . pipiens s.l. specimens that were trapped in theunderground cellar (n = 269) were also tested as these mightrepresent biotype molestus that is presumed to feed onmammals (Reusken et al ., 2010). The remainder of theCx . pipiens s.l. collection (n = 918) was not tested, astheir ornithophilic feeding behaviour and their prehibernationfeeding preferences for plant sugars make them unlikely tohave acquired SBV. Gonotrophic dissociation is considerednon-existent for Cx . pipiens (Mitchell & Briegel, 1989a, b).



Fig. 1. Locations of the confirmed Schmallenberg virus (SBV)-infected farms in the Netherlands where hibernating mosquitoes (Culicidae) werecollected. Per farm, the relative species composition is shown.

The same holds for Cx . territans , with the difference that thisspecies feeds primarily on amphibians (Hudson, 1986).

Total RNA was extracted (Scholte et al ., 2008) and analysedfor the presence of SBV genomic RNA using a real-time PCRfor S and L-segment (Bilk et al ., 2012; Hoffmann et al ., 2012).None of the 868 hibernating mosquitoes tested was foundpositive for SBV RNA.

Since its emergence in Europe, SBV has been detected infour Culicoides species: Culicoides obsoletus , C . scoticus , C .dewulfi , and C . chiopterus (De Regge et al ., 2012; Rasmussenet al ., 2012; Elbers et al ., 2013), which could represent themain vector species for SBV transmission. However, basedon the reported vectors for Simbu serogroup viruses, a roleof mosquitoes in the transmission cycle of SBV cannot beexcluded. In the present study, we did not find evidence forthe persistence of SBV in mosquitoes overwintering at SBV-affected animal holdings in the Netherlands. At the time of

writing, it was not known whether the virus has persisted untilthe next vector season in 2012 in the Netherlands. However,recent data suggest that SBV has persisted through the win-ter in France, the UK, Belgium, the Netherlands, Germany,Denmark and Switzerland as acute infections were found incattle in the spring, summer and/or autumn of 2012 (Anony-mous, 2012; S. Zientara, personal communication, 2012;R. Bødker, personal communication, 2012; Garigliany et al .,2012; ProMED-Mail, 2012d, e). Based on the reported infec-tion rates for WNV and SLEV in overwintering mosquitoes,which varied between 0.1% and 0.3% (Bailey et al ., 1978;Nasci et al ., 2001; Farajollahi et al ., 2005), a sample size of868 mosquitoes gives a probability varying between 58.1%and 92.6% to detect one or more positive mosquitoes, assum-ing a test sensitivity and specificity of 100% and that the testedmosquito species represent indeed SBV vector species. A morethorough study of the mosquito fauna at infected ruminant


No Schmallenberg virus in hibernating mosquitoes 5

farms in the period of high SBV circulation and during thewinter months is needed to gain insight in the possible role ofmosquitoes in SBV transmission and persistence. In addition,alternative overwintering strategies such as virus persistencein Culicoides larvae, in the ruminant hosts or persistence viaintra-uterine infected newborns, need to be investigated.

Acknowledgements

The authors wish to thank the farm owners to allow theresearchers collecting the hibernating mosquitoes on theirpremises, and Piet Vellema (GD, Deventer, the Netherlands)for contacting the farm owners. They also want to thank HelgeKampen (FLI, Germany) for supplying diagnostic referencematerial of An . maculipennis s.s., and Ivelina Staneva andFrans Jacobs (Wageningen University, the Netherlands) forcarrying out the molecular diagnostics on Maculipennis Groupmosquitoes.

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Accepted 11 November 2012


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