McCorkell, B.F

Mellor, D.J.

Palmarini, M.

Purse, B.V.

Shaw, A.E.

Shaw, P.E.

English

PubMed

A. E. Shaw

D. J. Mellor

B. V. Purse

P. E. Shaw

B. F. McCorkell

M. Palmarini

Crossref

Veterinary Record

Transmission of Schmallenberg virus in a housed dairy herd in the UK

Schmallenberg virus (SBV) is a recently emerged Orthobunyavirus of ruminants originally discovered in 2011 near the town of Schmallenberg in Germany (Hoffmann and others 2012). SBV appears to have entered Europe in the summer of 2011 and has since spread rapidly across much of central and northern Europe. Seroprevalence in some areas has been reported close to 100 per cent

(Tarlinton and others 2012, Meroc and others 2013). Viruses closely related to SBV are known to be transmitted by Culicoides biting midges (Jennings and Mellor 1989), and field studies have shown the presence of SBV RNA in Culicoides species in several affected countries

(Rasmussen and others 2012, Elbers and others 2013)

McCorkell, B.F.

NERC Open Research Archive

Short CommunicationShort CommunicationsDecember 21/28, 2013 | Veterinary RecordTransmission of Schmallenberg virus in a housed dairy herd in the UKA. E. Shaw, D. J. Mellor, B. V. Purse, P. E. Shaw, B. F. McCorkell, M. PalmariniSchmallenberg virus (SBV) is a recently emerged Orthobunyavirus of ruminants originally discovered in 2011 near the town of Schmallenberg in Germany (Hoffmann and others 2012). SBV appears to have entered Europe in the summer of 2011 and has since spread rapidly across much of central and northern Europe. Seroprevalence in some areas has been reported close to 100 per cent (Tarlinton and others 2012, Meroc and others 2013). Viruses closely related to SBV are known to be transmitted by Culicoides biting midges (Jennings and Mellor 1989), and field studies have shown the pres-ence of SBV RNA in Culicoides species in several affected countries (Rasmussen and others 2012, Elbers and others 2013).SBV infection is associated with abortion and malformations in cattle and sheep, and has been shown to be neurotropic in lambs and calves infected in utero (van den Brom and others 2012, Varela and others 2013). In dairy cattle, an ‘acute’ form of the disease associated with a drop in milk yield, diarrhoea and mild pyrexia has also been observed. Here we report a within-herd study on a typical dairy farm located in southern England during 2012. The farm runs a dairy herd comprising approximately 230 Holstein cows, approximately 150 of which represent a milking herd. Importantly, no animals were imported onto the farm during the period of this study.In February 2012, a cow (#157) aborted close to term. Suspecting SBV as the cause of abortion, we sampled the affected cow as well as nine additional animals using an indirect SBV antibody ELISA (IDvet). All animals were seronegative for SBV with the exception of cow #157 (Fig 1a). An identical result was obtained upon repeat testing using a second set of blood samples. We further confirmed the presence of anti-SBV antibodies by virus neutralisation assay (Loeffen and others 2012) (data not shown), and immunofluorescence using Short CommunicationA. E. Shaw, PhD,M. Palmarini, DVM PhD,MRC-University of Glasgow Centre for Virus Research, Institute of Infection, Immunity and Inflammation, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow G61 1QH, UKD. J. Mellor, BVMS PhD,Scottish Centre for Production Animal Health and Food Safety, Large Animal Clinical Sciences and Public Health, School of Veterinary Medicine, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow G61 1QH, UKB. V. Purse, PhD,Centre for Ecology & Hydrology, Bush Estate, Penicuik, Midlothian EH26 0QB, UKP. E. Shaw,Bishops Farm, Bushton, Swindon, Wiltshire, UKB. F. McCorkell, BVSc,The George Veterinary Group, High Street, Malmesbury, Wiltshire, UKE-mail for correspondence:  andrew.shaw@glasgow.ac.ukProvenance: Not commissioned; externally peer reviewedAccepted October 8, 2013Veterinary Record (2013) doi: 10.1136/vr.101983SBV or mock-infected BHK21 cells and sera from cow #157 (Fig 1b). Fluorescent signal was only observed in cells infected with SBV, while no cross-reaction was observed in uninfected cells. Together, these data indicate that SBV infection was present at least as far north as 51.5°N in the UK by February 2012, merely six to eight months after its first recorded appearance in Germany (Hoffmann and others 2012).Considering arbovirus replication within insect vectors, and the biting activity of the midges required for transmission is inherently reliant upon the ambient temperature, it is interesting to note that in the period immediately prior to the sampling of cow #157, the maxi-mum temperature only reached approximately 10°C (Fig 1c). Using isotype-specific antibody ELISAs, we found IgG but not IgM antibod-ies in the serum of cow #157 (data not shown). These data suggest cow #157 had been infected for more than 10–14 days prior to sam-pling, although it is difficult to speculate the exact time of infection.In May 2012 we screened the entire herd for the presence of SBV antibodies. Seroprevalence among all the animals tested in May was 1.7 per cent (n=232). Subsequently, we retested the herd in November 2012 (towards the end of the midge season), whereupon seropreva-lence had risen to 89.1 per cent (n=220, Fig 1e).During the period between spring and autumn samplings, numer-ous clinical cases similar to the ‘acute’ form of SBV infection were observed in the herd, with a sudden drop in milk yield for up to a week, followed by recovery, as described in other herds experiencing SBV infection. Similarly, a general increase in diarrhoea was observed among the herd during the summer period, although this observation is difficult to measure, may be multifactorial and retains an element of subjectivity. The dispersed nature of the episodes of acute disease suggests that the spread of infection proceeded over a protracted period of time, although it is difficult to retroactively diagnose acute SBV infection.Interestingly, the heavy rainfall during the summer period resulted in the milking herd being at pasture on only two occasions (in total four days between May 31 and June 2, and between June 21 and 23) in the whole of 2012. In the remaining time, the herd was housed in open-plan sheds used commonly in the UK, with openings that make them freely accessible to insects.The study reported here has uncovered valuable insights not nec-essarily revealed by national serosurveillance screens, and largely con-curs with data from other studies of SBV ((EFSA) 2013, Meroc and others 2013, Wernike and others 2013). However, in contrast with some studies, we found a large increase in SBV herd prevalence dur-ing a period in which many of the animals were housed (Tarlinton and Daly 2013). For exophilic species of midge, for example, Culicoides imicola (Kieffer), stabling during periods of vector activity has his-torically been used as a way in which to reduce transmission risk (Meiswinkel and others 2007, 2000). This study, as well as previ-ous reports during the recent Bluetongue virus epizootics, reaffirms that housing animals in farm buildings typical of those in the UK during periods of vector activity is not an effective measure against Culicoides-borne arbovirus infections in northern Europe, where the predominant Culicoides species are those of the C obsoletus species com-plex (Meiswinkel and others 2008, Baylis and others 2010, Viennet and others 2012). Heavy rain has been shown to suppress outdoors rather than indoors Culicoides activity (Baylis and others 2010), and it is therefore reasonable to suggest that substantial Culicoides-borne SBV transmission occurred inside the sheds during the summer of 2012. Clearly, outbreaks of arboviral diseases can still occur even when animals are not at pasture. It remains possible that significant ‘midge-proofing’ of buildings may offer some protection from midge-borne transmission, although this is likely to additionally depend upon climatic variables, the local landscape and husbandry practices. Further work is required to determine whether such measures are eco-nomically viable and the contexts in which they are effective.Interestingly, the first case (cow #157) identified at this farm was diagnosed in February 2012. Therefore, cow #157 must have been infected either during the winter, when the outside temperature was  on September 16, 2019 by guest. Protected by copyright.http://veterinaryrecord.bmj.com/Veterinary Record: first published as 10.1136/vr.101983 on 6 November 2013. Downloaded from Short CommunicationShort CommunicationVeterinary Record | December 21/28, 2013never above 10°C, or in the summer/autumn of 2011 before or soon after the discovery of SBV in Germany.Open Access This is an Open Access article distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 3.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial.  See: http://creativecommons.org/licenses/by-nc/3.0/AcknowledgementsThe authors wish to thank the farm staff at Bishops Farm for their help in collecting samples. This work was funded by the BBSRC and the Wellcome Trust.ReferencesBAYLIS, M., PARKIN, H., KREPPEL, K., CARPENTER, S., MELLOR, P. S. & MCINTYRE, K. M. (2010) Evaluation of housing as a means to protect cattle from Culicoides biting midges, the vectors of bluetongue virus. Medical and Veterinary Entomology 24, 38–45(EFSA), E. F. S. A. (2013) Technical report: “Schmallenberg” virus: analysis of the epide-miological dataELBERS, A. R., MEISWINKEL, R., VAN WEEZEP, E., SLOET VAN OLDRUITENBORGH-OOSTERBAAN, M. M. & KOOI, E. A. (2013) Schmallenberg virus in Culicoides spp. Biting midges, the Netherlands, 2011. Emerging Infectious Diseases 19, 106–109HOFFMANN, B., SCHEUCH, M., HOPER, D., JUNGBLUT, R., HOLSTEG, M., SCHIRRMEIER, H., ESCHBAUMER, M., GOLLER, K. V., WERNIKE, K., FISCHER, M., BREITHAUPT, A., METTENLEITER, T. C. & BEER, M. (2012) Novel orthobun-yavirus in Cattle, Europe, 2011. Emerging Infectious Diseases 18, 469–472150100500S/P (%)11 155 157 193 221 465 472 486 734 735cow number70%SBV infected uninfected302520151050-5-10-15Feb Mar Apr May Jun Jul Aug Sep Oct Nov DecDaily maximumDaily minimumcow #157positive Screen 1 Screen 2Temperature (°C)Springn = 232Autumnn = 220positivenegativeinconclusive(a)(c)(d)(b)FIG 1: (a) Sera of a selection of cattle tested for the presence of antibodies to Schmallenberg virus (SBV) in February 2012.  Sample-to-positive ratios (S/P) are expressed as percentages and values >70 per cent are regarded as positive. All animals were negative with the exception of cow #157. (b) SBV infected (left) and uninfected (right) BHK21 cells were immunolabelled with sera from cow #157 and analysed by immunofluorescence microscopy. Fluorescent signal was only observed in cells infected with SBV. Bar = 10µm. (c) Maximum and minimum daily temperatures for the period February–December 2012 at the nearest weather station (Lyneham, approximately 4.8 km from the farm described in this study), with arrows indicating dates of significance during this study. Data were obtained from the UK Meteorological Office, Met Office Integrated Data Archive System (MIDAS) Land and Marine Surface Stations Data (1853-current), NCAS British Atmospheric Data Centre, 2012. ‘Screen 1’ and ‘Screen 2’ represent the points of whole-herd screening for SBV antibodies. (d) Seroprevalence was determined for the entire herd in the spring (May) and autumn (November) 2012, and was found to rise from  1.7 per cent in the spring to 89.1 per cent in the autumn. on September 16, 2019 by guest. Protected by copyright.http://veterinaryrecord.bmj.com/Veterinary Record: first published as 10.1136/vr.101983 on 6 November 2013. Downloaded from Short CommunicationDecember 21/28, 2013 | Veterinary RecordJENNINGS, M. & MELLOR, P. S. (1989) Culicoides: biological vectors of Akabane virus. Veterinary Microbiology 21, 125–131LOEFFEN, W., QUAK, S., DE BOER-LUIJTZE, E., HULST, M., VAN DER POEL, W., BOUWSTRA, R. & MAAS, R. (2012) Development of a virus neutralisation test to detect antibodies against Schmallenberg virus and serological results in suspect and infected herds. Acta Veterinaria Scandinavica 54, 44MEISWINKEL, R., BALDET, T., DE DEKEN, R., TAKKEN, W., DEL’ECOLLE, J. C. & MELLOR, P. S. (2007) Epidemiological Analysis of the 2006 Bluetongue Virus Serotype 8 Epidemic in North-Western Europe: Distribution and Dynamics of Vector Species. Parma: European Food Safety AuthorityMEISWINKEL, R., BALDET, T., DE DEKEN, R., TAKKEN, W., DELECOLLE, J. C. & MELLOR, P. S. (2008) The 2006 outbreak of bluetongue in northern Europe-the entomological perspective. Preventive Veterinary Medicine 87, 55–63MEISWINKEL, R., BAYLIS, M. & LABUSCHAGNE, K. (2000) Stabling and the protec-tion of horses from Culicoides bolitinos (Diptera: Ceratopogonidae), a recently identi-fied vector of African horse sickness. Bulletin of Entomological Research 90, 509–515MEROC, E., POSKIN, A., VAN LOO, H., QUINET, C., VAN DRIESSCHE, E., DELOOZ, L., BEHAEGHEL, I., RIOCREUX, F., HOOYBERGHS, J., DE REGGE, N., CAIJ, A. B., VAN DEN BERG, T. & VAN DER STEDE, Y. (2013) Large-scale cross-sectional serological survey of schmallenberg virus in belgian cattle at the end of the first vector season. Transbound Emergency Disease 60, 4–8RASMUSSEN, L., KRISTENSEN, B., KIRKEBY, C., RASMUSSEN, T. B., BELSHAM, G. J., BØDKER, R., BØTNER, A. (2012) Culicoids as vectors of schmallenberg virus. Emerging Infectious Diseases 18, 1204–1206TARLINTON, R. & DALY, J. (2013) Testing for Schmallenberg virus. The Veterinary Record 172, 190TARLINTON, R., DALY, J., DUNHAM, S. & KYDD, J. (2012) The challenge of Schmallenberg virus emergence in Europe. Veterinary Journal 194, 10–18VAN DEN BROM, R., LUTTIKHOLT, S. J., LIEVAART-PETERSON, K., PEPERKAMP, N. H., MARS, M. H., VAN DER POEL, W. H. & VELLEMA, P. (2012) Epizootic of ovine congenital malformations associated with Schmallenberg virus infection. Tijdschrift Voor Diergeneeskunde 137, 106–111VARELA, M., SCHNETTLER, E., CAPORALE, M., MURGIA, C., BARRY, G., MCFARLANE, M., MCGREGOR, E., PIRAS, I. M., SHAW, A., LAMM, C., JANOWICZ, A., BEER, M., GLASS, M., HERDER, V., HAHN, K., BAUMGARTNER, W., KOHL, A. & PALMARINI, M. (2013) Schmallenberg virus pathogenesis, tropism and interaction with the innate immune system of the host. PLoS Pathogens 9, e1003133VIENNET, E., GARROS, C., RAKOTOARIVONY, I., ALLENE, X., GARDES, L., LHOIR, J., FUENTES, I., VENAIL, R., CROCHET, D., LANCELOT, R., RIOU, M., MOULIA, C., BALDET, T. & BALENGHIEN, T. (2012) Host-seeking activity of bluetongue virus vectors: endo/exophagy and circadian rhythm of culicoides in Western Europe. PLoS ONE 7, e48120WERNIKE, K., KOHN, M., CONRATHS, F. J., WERNER, D., KAMEKE, D., HECHINGER, S., KAMPEN, H. & BEER, M. (2013) Transmission of Schmallenberg Virus during Winter, Germany. Emerging Infectious Diseases 19, 1701–1703 on September 16, 2019 by guest. Protected by copyright.http://veterinaryrecord.bmj.com/Veterinary Record: first published as 10.1136/vr.101983 on 6 November 2013. Downloaded from 

Enlighten

    Shaw, A.E., Mellor, D.J., Purse, B.V., Shaw, P.E., McCorkell, B.F, and Palmarini, M. (2013) Transmission of Schmallenberg virus in a housed dairy herd in the UK. Veterinary Record, 173 (24). p. 609.   Copyright © 2013 The Authors    http://eprints.gla.ac.uk/89933    Deposited on:  23 January 2014                          Enlighten – Research publications by members of the University of Glasgow http://eprints.gla.ac.uk Short CommunicationShort CommunicationsDecember 21/28, 2013 | Veterinary RecordTransmission of Schmallenberg virus in a housed dairy herd in the UKA. E. Shaw, D. J. Mellor, B. V. Purse, P. E. Shaw, B. F. McCorkell, M. PalmariniSchmallenberg virus (SBV) is a recently emerged Orthobunyavirus of ruminants originally discovered in 2011 near the town of Schmallenberg in Germany (Hoffmann and others 2012). SBV appears to have entered Europe in the summer of 2011 and has since spread rapidly across much of central and northern Europe. Seroprevalence in some areas has been reported close to 100 per cent (Tarlinton and others 2012, Meroc and others 2013). Viruses closely related to SBV are known to be transmitted by Culicoides biting midges (Jennings and Mellor 1989), and field studies have shown the pres-ence of SBV RNA in Culicoides species in several affected countries (Rasmussen and others 2012, Elbers and others 2013).SBV infection is associated with abortion and malformations in cattle and sheep, and has been shown to be neurotropic in lambs and calves infected in utero (van den Brom and others 2012, Varela and others 2013). In dairy cattle, an ‘acute’ form of the disease associated with a drop in milk yield, diarrhoea and mild pyrexia has also been observed. Here we report a within-herd study on a typical dairy farm located in southern England during 2012. The farm runs a dairy herd comprising approximately 230 Holstein cows, approximately 150 of which represent a milking herd. Importantly, no animals were imported onto the farm during the period of this study.In February 2012, a cow (#157) aborted close to term. Suspecting SBV as the cause of abortion, we sampled the affected cow as well as nine additional animals using an indirect SBV antibody ELISA (IDvet). All animals were seronegative for SBV with the exception of cow #157 (Fig 1a). An identical result was obtained upon repeat testing using a second set of blood samples. We further confirmed the presence of anti-SBV antibodies by virus neutralisation assay (Loeffen and others 2012) (data not shown), and immunofluorescence using Short CommunicationA. E. Shaw, PhD,M. Palmarini, DVM PhD,MRC-University of Glasgow Centre for Virus Research, Institute of Infection, Immunity and Inflammation, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow G61 1QH, UKD. J. Mellor, BVMS PhD,Scottish Centre for Production Animal Health and Food Safety, Large Animal Clinical Sciences and Public Health, School of Veterinary Medicine, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow G61 1QH, UKB. V. Purse, PhD,Centre for Ecology & Hydrology, Bush Estate, Penicuik, Midlothian EH26 0QB, UKP. E. Shaw,Bishops Farm, Bushton, Swindon, Wiltshire, UKB. F. McCorkell, BVSc,The George Veterinary Group, High Street, Malmesbury, Wiltshire, UKE-mail for correspondence:  andrew.shaw@glasgow.ac.ukProvenance: Not commissioned; externally peer reviewedAccepted October 8, 2013Veterinary Record (2013) doi: 10.1136/vr.101983SBV or mock-infected BHK21 cells and sera from cow #157 (Fig 1b). Fluorescent signal was only observed in cells infected with SBV, while no cross-reaction was observed in uninfected cells. Together, these data indicate that SBV infection was present at least as far north as 51.5°N in the UK by February 2012, merely six to eight months after its first recorded appearance in Germany (Hoffmann and others 2012).Considering arbovirus replication within insect vectors, and the biting activity of the midges required for transmission is inherently reliant upon the ambient temperature, it is interesting to note that in the period immediately prior to the sampling of cow #157, the maxi-mum temperature only reached approximately 10°C (Fig 1c). Using isotype-specific antibody ELISAs, we found IgG but not IgM antibod-ies in the serum of cow #157 (data not shown). These data suggest cow #157 had been infected for more than 10–14 days prior to sam-pling, although it is difficult to speculate the exact time of infection.In May 2012 we screened the entire herd for the presence of SBV antibodies. Seroprevalence among all the animals tested in May was 1.7 per cent (n=232). Subsequently, we retested the herd in November 2012 (towards the end of the midge season), whereupon seropreva-lence had risen to 89.1 per cent (n=220, Fig 1e).During the period between spring and autumn samplings, numer-ous clinical cases similar to the ‘acute’ form of SBV infection were observed in the herd, with a sudden drop in milk yield for up to a week, followed by recovery, as described in other herds experiencing SBV infection. Similarly, a general increase in diarrhoea was observed among the herd during the summer period, although this observation is difficult to measure, may be multifactorial and retains an element of subjectivity. The dispersed nature of the episodes of acute disease suggests that the spread of infection proceeded over a protracted period of time, although it is difficult to retroactively diagnose acute SBV infection.Interestingly, the heavy rainfall during the summer period resulted in the milking herd being at pasture on only two occasions (in total four days between May 31 and June 2, and between June 21 and 23) in the whole of 2012. In the remaining time, the herd was housed in open-plan sheds used commonly in the UK, with openings that make them freely accessible to insects.The study reported here has uncovered valuable insights not nec-essarily revealed by national serosurveillance screens, and largely con-curs with data from other studies of SBV ((EFSA) 2013, Meroc and others 2013, Wernike and others 2013). However, in contrast with some studies, we found a large increase in SBV herd prevalence dur-ing a period in which many of the animals were housed (Tarlinton and Daly 2013). For exophilic species of midge, for example, Culicoides imicola (Kieffer), stabling during periods of vector activity has his-torically been used as a way in which to reduce transmission risk (Meiswinkel and others 2007, 2000). This study, as well as previ-ous reports during the recent Bluetongue virus epizootics, reaffirms that housing animals in farm buildings typical of those in the UK during periods of vector activity is not an effective measure against Culicoides-borne arbovirus infections in northern Europe, where the predominant Culicoides species are those of the C obsoletus species com-plex (Meiswinkel and others 2008, Baylis and others 2010, Viennet and others 2012). Heavy rain has been shown to suppress outdoors rather than indoors Culicoides activity (Baylis and others 2010), and it is therefore reasonable to suggest that substantial Culicoides-borne SBV transmission occurred inside the sheds during the summer of 2012. Clearly, outbreaks of arboviral diseases can still occur even when animals are not at pasture. It remains possible that significant ‘midge-proofing’ of buildings may offer some protection from midge-borne transmission, although this is likely to additionally depend upon climatic variables, the local landscape and husbandry practices. Further work is required to determine whether such measures are eco-nomically viable and the contexts in which they are effective.Interestingly, the first case (cow #157) identified at this farm was diagnosed in February 2012. Therefore, cow #157 must have been infected either during the winter, when the outside temperature was  group.bmj.com on January 23, 2014 - Published by veterinaryrecord.bmj.comDownloaded from Short CommunicationShort CommunicationVeterinary Record | December 21/28, 2013never above 10°C, or in the summer/autumn of 2011 before or soon after the discovery of SBV in Germany.Open Access This is an Open Access article distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 3.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial.  See: http://creativecommons.org/licenses/by-nc/3.0/AcknowledgementsThe authors wish to thank the farm staff at Bishops Farm for their help in collecting samples. This work was funded by the BBSRC and the Wellcome Trust.ReferencesBAYLIS, M., PARKIN, H., KREPPEL, K., CARPENTER, S., MELLOR, P. S. & MCINTYRE, K. M. (2010) Evaluation of housing as a means to protect cattle from Culicoides biting midges, the vectors of bluetongue virus. Medical and Veterinary Entomology 24, 38–45(EFSA), E. F. S. A. (2013) Technical report: “Schmallenberg” virus: analysis of the epide-miological dataELBERS, A. R., MEISWINKEL, R., VAN WEEZEP, E., SLOET VAN OLDRUITENBORGH-OOSTERBAAN, M. M. & KOOI, E. A. (2013) Schmallenberg virus in Culicoides spp. Biting midges, the Netherlands, 2011. Emerging Infectious Diseases 19, 106–109HOFFMANN, B., SCHEUCH, M., HOPER, D., JUNGBLUT, R., HOLSTEG, M., SCHIRRMEIER, H., ESCHBAUMER, M., GOLLER, K. V., WERNIKE, K., FISCHER, M., BREITHAUPT, A., METTENLEITER, T. C. & BEER, M. (2012) Novel orthobun-yavirus in Cattle, Europe, 2011. Emerging Infectious Diseases 18, 469–472150100500S/P (%)11 155 157 193 221 465 472 486 734 735cow number70%SBV infected uninfected302520151050-5-10-15Feb Mar Apr May Jun Jul Aug Sep Oct Nov DecDaily maximumDaily minimumcow #157positive Screen 1 Screen 2Temperature (°C)Springn = 232Autumnn = 220positivenegativeinconclusive(a)(c)(d)(b)FIG 1: (a) Sera of a selection of cattle tested for the presence of antibodies to Schmallenberg virus (SBV) in February 2012.  Sample-to-positive ratios (S/P) are expressed as percentages and values >70 per cent are regarded as positive. All animals were negative with the exception of cow #157. (b) SBV infected (left) and uninfected (right) BHK21 cells were immunolabelled with sera from cow #157 and analysed by immunofluorescence microscopy. Fluorescent signal was only observed in cells infected with SBV. Bar = 10µm. (c) Maximum and minimum daily temperatures for the period February–December 2012 at the nearest weather station (Lyneham, approximately 4.8 km from the farm described in this study), with arrows indicating dates of significance during this study. Data were obtained from the UK Meteorological Office, Met Office Integrated Data Archive System (MIDAS) Land and Marine Surface Stations Data (1853-current), NCAS British Atmospheric Data Centre, 2012. ‘Screen 1’ and ‘Screen 2’ represent the points of whole-herd screening for SBV antibodies. (d) Seroprevalence was determined for the entire herd in the spring (May) and autumn (November) 2012, and was found to rise from  1.7 per cent in the spring to 89.1 per cent in the autumn. group.bmj.com on January 23, 2014 - Published by veterinaryrecord.bmj.comDownloaded from Short CommunicationDecember 21/28, 2013 | Veterinary RecordJENNINGS, M. & MELLOR, P. S. (1989) Culicoides: biological vectors of Akabane virus. Veterinary Microbiology 21, 125–131LOEFFEN, W., QUAK, S., DE BOER-LUIJTZE, E., HULST, M., VAN DER POEL, W., BOUWSTRA, R. & MAAS, R. (2012) Development of a virus neutralisation test to detect antibodies against Schmallenberg virus and serological results in suspect and infected herds. Acta Veterinaria Scandinavica 54, 44MEISWINKEL, R., BALDET, T., DE DEKEN, R., TAKKEN, W., DEL’ECOLLE, J. C. & MELLOR, P. S. (2007) Epidemiological Analysis of the 2006 Bluetongue Virus Serotype 8 Epidemic in North-Western Europe: Distribution and Dynamics of Vector Species. Parma: European Food Safety AuthorityMEISWINKEL, R., BALDET, T., DE DEKEN, R., TAKKEN, W., DELECOLLE, J. C. & MELLOR, P. S. (2008) The 2006 outbreak of bluetongue in northern Europe-the entomological perspective. Preventive Veterinary Medicine 87, 55–63MEISWINKEL, R., BAYLIS, M. & LABUSCHAGNE, K. (2000) Stabling and the protec-tion of horses from Culicoides bolitinos (Diptera: Ceratopogonidae), a recently identi-fied vector of African horse sickness. Bulletin of Entomological Research 90, 509–515MEROC, E., POSKIN, A., VAN LOO, H., QUINET, C., VAN DRIESSCHE, E., DELOOZ, L., BEHAEGHEL, I., RIOCREUX, F., HOOYBERGHS, J., DE REGGE, N., CAIJ, A. B., VAN DEN BERG, T. & VAN DER STEDE, Y. (2013) Large-scale cross-sectional serological survey of schmallenberg virus in belgian cattle at the end of the first vector season. Transbound Emergency Disease 60, 4–8RASMUSSEN, L., KRISTENSEN, B., KIRKEBY, C., RASMUSSEN, T. B., BELSHAM, G. J., BØDKER, R., BØTNER, A. (2012) Culicoids as vectors of schmallenberg virus. Emerging Infectious Diseases 18, 1204–1206TARLINTON, R. & DALY, J. (2013) Testing for Schmallenberg virus. The Veterinary Record 172, 190TARLINTON, R., DALY, J., DUNHAM, S. & KYDD, J. (2012) The challenge of Schmallenberg virus emergence in Europe. Veterinary Journal 194, 10–18VAN DEN BROM, R., LUTTIKHOLT, S. J., LIEVAART-PETERSON, K., PEPERKAMP, N. H., MARS, M. H., VAN DER POEL, W. H. & VELLEMA, P. (2012) Epizootic of ovine congenital malformations associated with Schmallenberg virus infection. Tijdschrift Voor Diergeneeskunde 137, 106–111VARELA, M., SCHNETTLER, E., CAPORALE, M., MURGIA, C., BARRY, G., MCFARLANE, M., MCGREGOR, E., PIRAS, I. M., SHAW, A., LAMM, C., JANOWICZ, A., BEER, M., GLASS, M., HERDER, V., HAHN, K., BAUMGARTNER, W., KOHL, A. & PALMARINI, M. (2013) Schmallenberg virus pathogenesis, tropism and interaction with the innate immune system of the host. PLoS Pathogens 9, e1003133VIENNET, E., GARROS, C., RAKOTOARIVONY, I., ALLENE, X., GARDES, L., LHOIR, J., FUENTES, I., VENAIL, R., CROCHET, D., LANCELOT, R., RIOU, M., MOULIA, C., BALDET, T. & BALENGHIEN, T. (2012) Host-seeking activity of bluetongue virus vectors: endo/exophagy and circadian rhythm of culicoides in Western Europe. PLoS ONE 7, e48120WERNIKE, K., KOHN, M., CONRATHS, F. J., WERNER, D., KAMEKE, D., HECHINGER, S., KAMPEN, H. & BEER, M. (2013) Transmission of Schmallenberg Virus during Winter, Germany. Emerging Infectious Diseases 19, 1701–1703 group.bmj.com on January 23, 2014 - Published by veterinaryrecord.bmj.comDownloaded from doi: 10.1136/vr.1019836, 2013 2013 173: 609 originally published online NovemberVeterinary Record A. E. Shaw, D. J. Mellor, B. V. Purse, et al. housed dairy herd in the UKTransmission of Schmallenberg virus in a http://veterinaryrecord.bmj.com/content/173/24/609.2.full.htmlUpdated information and services can be found at: These include:Open Accesshttp://creativecommons.org/licenses/by/3.0/commercial use, provided the original work is properly cited. See:others to distribute, remix, adapt and build upon this work, for permitsof the Creative Commons Attribution (CC BY 3.0) license, which This is an Open Access article distributed in accordance with the termsserviceEmail alertingthe box at the top right corner of the online article.Receive free email alerts when new articles cite this article. Sign up inCollectionsTopic (37 articles)Open access    Articles on similar topics can be found in the following collectionsNotes http://group.bmj.com/group/rights-licensing/permissionsTo request permissions go to: http://journals.bmj.com/cgi/reprintformTo order reprints go to: http://group.bmj.com/subscribe/To subscribe to BMJ go to: group.bmj.com on January 23, 2014 - Published by veterinaryrecord.bmj.comDownloaded from 

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Shaw, A.E., Mellor, D.J., Purse, B.V., Shaw, P.E., McCorkell, B.F, and 
Palmarini, M. (2013) Transmission of Schmallenberg virus in a housed dairy 
herd in the UK. Veterinary Record, 173 (24). p. 609. 
 
 
Copyright © 2013 The Authors 
 
 
 
http://eprints.gla.ac.uk/89933 
 
 
 
Deposited on:  23 January 2014 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
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Short CommunicationShort Communications
December 21/28, 2013 | Veterinary Record
Transmission of 
Schmallenberg virus 
in a housed dairy herd 
in the UK
A. E. Shaw, D. J. Mellor, B. V. Purse, 
P. E. Shaw, B. F. McCorkell, M. Palmarini
Schmallenberg virus (SBV) is a recently emerged Orthobunyavirus 
of ruminants originally discovered in 2011 near the town of 
Schmallenberg in Germany (Hoffmann and others 2012). SBV 
appears to have entered Europe in the summer of 2011 and has 
since spread rapidly across much of central and northern Europe. 
Seroprevalence in some areas has been reported close to 100 per cent 
(Tarlinton and others 2012, Meroc and others 2013). Viruses closely 
related to SBV are known to be transmitted by Culicoides biting midges 
(Jennings and Mellor 1989), and field studies have shown the pres-
ence of SBV RNA in Culicoides species in several affected countries 
(Rasmussen and others 2012, Elbers and others 2013).
SBV infection is associated with abortion and malformations in 
cattle and sheep, and has been shown to be neurotropic in lambs and 
calves infected in utero (van den Brom and others 2012, Varela and 
others 2013). In dairy cattle, an ‘acute’ form of the disease associated 
with a drop in milk yield, diarrhoea and mild pyrexia has also been 
observed. Here we report a within-herd study on a typical dairy farm 
located in southern England during 2012. The farm runs a dairy herd 
comprising approximately 230 Holstein cows, approximately 150 
of which represent a milking herd. Importantly, no animals were 
imported onto the farm during the period of this study.
In February 2012, a cow (#157) aborted close to term. Suspecting 
SBV as the cause of abortion, we sampled the affected cow as well 
as nine additional animals using an indirect SBV antibody ELISA 
(IDvet). All animals were seronegative for SBV with the exception 
of cow #157 (Fig 1a). An identical result was obtained upon repeat 
testing using a second set of blood samples. We further confirmed the 
presence of anti-SBV antibodies by virus neutralisation assay (Loeffen 
and others 2012) (data not shown), and immunofluorescence using 
Short Communication
A. E. Shaw, PhD,
M. Palmarini, DVM PhD,
MRC-University of Glasgow Centre for 
Virus Research, Institute of Infection, 
Immunity and Inflammation, College of 
Medical, Veterinary and Life Sciences, 
University of Glasgow, Glasgow G61 
1QH, UK
D. J. Mellor, BVMS PhD,
Scottish Centre for Production Animal 
Health and Food Safety, Large Animal 
Clinical Sciences and Public Health, 
School of Veterinary Medicine, 
College of Medical, Veterinary and 
Life Sciences, University of Glasgow, 
Glasgow G61 1QH, UK
B. V. Purse, PhD,
Centre for Ecology & Hydrology, Bush 
Estate, Penicuik, Midlothian EH26 0QB, 
UK
P. E. Shaw,
Bishops Farm, Bushton, Swindon, 
Wiltshire, UK
B. F. McCorkell, BVSc,
The George Veterinary Group, High 
Street, Malmesbury, Wiltshire, UK
E-mail for correspondence:  
andrew.shaw@glasgow.ac.uk
Provenance: Not commissioned; 
externally peer reviewed
Accepted October 8, 2013
Veterinary Record (2013) doi: 10.1136/vr.101983
SBV or mock-infected BHK21 cells and sera from cow #157 (Fig 1b). 
Fluorescent signal was only observed in cells infected with SBV, while 
no cross-reaction was observed in uninfected cells. Together, these data 
indicate that SBV infection was present at least as far north as 51.5°N 
in the UK by February 2012, merely six to eight months after its first 
recorded appearance in Germany (Hoffmann and others 2012).
Considering arbovirus replication within insect vectors, and the 
biting activity of the midges required for transmission is inherently 
reliant upon the ambient temperature, it is interesting to note that in 
the period immediately prior to the sampling of cow #157, the maxi-
mum temperature only reached approximately 10°C (Fig 1c). Using 
isotype-specific antibody ELISAs, we found IgG but not IgM antibod-
ies in the serum of cow #157 (data not shown). These data suggest 
cow #157 had been infected for more than 10–14 days prior to sam-
pling, although it is difficult to speculate the exact time of infection.
In May 2012 we screened the entire herd for the presence of SBV 
antibodies. Seroprevalence among all the animals tested in May was 
1.7 per cent (n=232). Subsequently, we retested the herd in November 
2012 (towards the end of the midge season), whereupon seropreva-
lence had risen to 89.1 per cent (n=220, Fig 1e).
During the period between spring and autumn samplings, numer-
ous clinical cases similar to the ‘acute’ form of SBV infection were 
observed in the herd, with a sudden drop in milk yield for up to a week, 
followed by recovery, as described in other herds experiencing SBV 
infection. Similarly, a general increase in diarrhoea was observed among 
the herd during the summer period, although this observation is difficult 
to measure, may be multifactorial and retains an element of subjectivity. 
The dispersed nature of the episodes of acute disease suggests that the 
spread of infection proceeded over a protracted period of time, although 
it is difficult to retroactively diagnose acute SBV infection.
Interestingly, the heavy rainfall during the summer period resulted 
in the milking herd being at pasture on only two occasions (in total 
four days between May 31 and June 2, and between June 21 and 23) 
in the whole of 2012. In the remaining time, the herd was housed in 
open-plan sheds used commonly in the UK, with openings that make 
them freely accessible to insects.
The study reported here has uncovered valuable insights not nec-
essarily revealed by national serosurveillance screens, and largely con-
curs with data from other studies of SBV ((EFSA) 2013, Meroc and 
others 2013, Wernike and others 2013). However, in contrast with 
some studies, we found a large increase in SBV herd prevalence dur-
ing a period in which many of the animals were housed (Tarlinton 
and Daly 2013). For exophilic species of midge, for example, Culicoides 
imicola (Kieffer), stabling during periods of vector activity has his-
torically been used as a way in which to reduce transmission risk 
(Meiswinkel and others 2007, 2000). This study, as well as previ-
ous reports during the recent Bluetongue virus epizootics, reaffirms 
that housing animals in farm buildings typical of those in the UK 
during periods of vector activity is not an effective measure against 
Culicoides-borne arbovirus infections in northern Europe, where the 
predominant Culicoides species are those of the C obsoletus species com-
plex (Meiswinkel and others 2008, Baylis and others 2010, Viennet 
and others 2012). Heavy rain has been shown to suppress outdoors 
rather than indoors Culicoides activity (Baylis and others 2010), and 
it is therefore reasonable to suggest that substantial Culicoides-borne 
SBV transmission occurred inside the sheds during the summer of 
2012. Clearly, outbreaks of arboviral diseases can still occur even 
when animals are not at pasture. It remains possible that significant 
‘midge-proofing’ of buildings may offer some protection from midge-
borne transmission, although this is likely to additionally depend 
upon climatic variables, the local landscape and husbandry practices. 
Further work is required to determine whether such measures are eco-
nomically viable and the contexts in which they are effective.
Interestingly, the first case (cow #157) identified at this farm was 
diagnosed in February 2012. Therefore, cow #157 must have been 
infected either during the winter, when the outside temperature was 
 group.bmj.com on January 23, 2014 - Published by veterinaryrecord.bmj.comDownloaded from 
Short CommunicationShort Communication
Veterinary Record | December 21/28, 2013
never above 10°C, or in the summer/autumn of 2011 before or soon 
after the discovery of SBV in Germany.
Open Access This is an Open Access article distributed in accordance with the 
Creative Commons Attribution Non Commercial (CC BY-NC 3.0) license, which permits 
others to distribute, remix, adapt, build upon this work non-commercially, and license 
their derivative works on different terms, provided the original work is properly cited 
and the use is non-commercial.  See: http://creativecommons.org/licenses/by-nc/3.0/
Acknowledgements
The authors wish to thank the farm staff at Bishops Farm for their 
help in collecting samples. This work was funded by the BBSRC and 
the Wellcome Trust.
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150
100
50
0
S/
P 
(%
)
11 155 157 193 221 465 472 486 734 735
cow number
70%
SBV infected uninfected
30
25
20
15
10
5
0
-5
-10
-15
Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec
Daily maximum
Daily minimum
cow #157
positive Screen 1 Screen 2
Te
m
pe
ra
tu
re
 (°
C)
Spring
n = 232
Autumn
n = 220
positive
negative
inconclusive
(a)
(c)
(d)
(b)
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1701–1703
 group.bmj.com on January 23, 2014 - Published by veterinaryrecord.bmj.comDownloaded from 
doi: 10.1136/vr.101983
6, 2013
 2013 173: 609 originally published online NovemberVeterinary Record
 
A. E. Shaw, D. J. Mellor, B. V. Purse, et al.
 
housed dairy herd in the UK
Transmission of Schmallenberg virus in a
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(d) Seroprevalence was determined for the entire herd in the spring (May) and autumn

Development of a virus neutralisation test to detect antibodies against Schmallenberg virus and serological results in suspect and infected herds.

Epidemiological Analysis of the 2006 Bluetongue Virus Serotype 8 Epidemic in North-Western Europe: Distribution and Dynamics of Vector Species. Parma: European Food Safety Authority

Evaluation of housing as a means to protect cattle from Culicoides biting midges, the vectors of bluetongue virus. Medical and Veterinary Entomology 24,

Host-seeking activity of bluetongue virus vectors: endo/exophagy and circadian rhythm of culicoides in

Schmallenberg virus pathogenesis, tropism and interaction with the innate immune system of the host.

T esting for Schmallenberg virus. The Veterinary Record 172,

http://nora.nerc.ac.uk/id/eprint/522562/1/N522562JA.pdf

Transmission of Schmallenberg virus in a housed dairy herd in the UK

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