DISPATCHESFigure 2. Detection of Schmallenberg virus genome in the bloodof experimentally infected cattle and sheep, Germany, 2014.(14,15); further reasons for the unexpected recurrence ofSBV could be persistence within the insect vectors. Asa consequence, the infection of naive animals in autumn2014 resulted in an increasing frequency of the birth ofmalformed offspring in the following winter.AcknowledgmentsWe thank the German local diagnostic laboratories for providingthe SBV-positive samples. We are grateful to Kristin Tripplerfor excellent technical assistance. We gratefully acknowledgeAndrea Aebischer’s help with the animal experiment and thededicated animal care by staff of the isolation unit of theFriedrich-Loeffler-Institut. We also thank Andreas Moss forproviding SBV isolate D495/12-1.This work was financially supported by Boehringer IngelheimVetmedica GmbH.Dr. Wernike is a veterinarian and scientist at the Friedrich-Loeffler-Institut, Institute of Diagnostic Virology. Her researchinterests are emerging animal viruses, molecular diagnostics,and pathogenesis.References1. Hoffmann B, Scheuch M, Höper D, Jungblut R, Holsteg M,Schirrmeier H, et al. Novel orthobunyavirus in cattle, Europe,2011. Emerg Infect Dis. 2012;18:469–72. http://dx.doi.org/10.3201/eid1803.1119052. Beer M, Conraths FJ, van der Poel WH. “Schmallenberg virus”—a novel orthobunyavirus emerging in Europe. Epidemiol Infect.2013;141:1–8. http://dx.doi.org/10.1017/S09502688120022453. Wernike K, Conraths F, Zanella G, Granzow H, Gache K,Schirrmeier H, et al. Schmallenberg virus—two years ofexperiences. Prev Vet Med. 2014;116:423–34. http://dx.doi.org/10.1016/j.prevetmed.2014.03.0214. Conraths FJ, Kamer D, Teske K, Hoffmann B, Mettenleiter TC,Beer M. Reemerging Schmallenberg virus infections, Germany,2012. Emerg Infect Dis. 2013;19:513–4. http://dx.doi.org/10.3201/eid1903.1213245. Friedrich-Loeffler-Institut. Schmallenberg virus [2015 Feb 4].http://www.fli.bund.de/en/startseite/current-news/animal-diseasesituation/new-orthobunyavirus-detected-in-cattle-in-germany.html6. Macmachlan NJ, Mayo CE. Potential strategies for control of bluetongue,a globally emerging, Culicoides-transmitted viral diseaseof ruminant livestock and wildlife. Antiviral Res. 2013;99:79–90.http://dx.doi.org/10.1016/j.antiviral.2013.04.0217. Fischer M, Hoffmann B, Goller KV, Höper D, Wernike K, Beer M.A mutation “hot spot” in the Schmallenberg virus M segment. J GenVirol. 2013;94:1161–7. http://dx.doi.org/10.1099/vir.0.049908-08. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S.MEGA5: molecular evolutionary genetics analysis using maximumlikelihood, evolutionary distance, and maximum parsimonymethods. Mol Biol Evol. 2011;28:2731–9. http://dx.doi.org/10.1093/molbev/msr1219. Coupeau D, Claine F, Wiggers L, Kirschvink N, Muylkens B.In vivo and in vitro identification of a hypervariable region inSchmallenberg virus. J Gen Virol. 2013;94:1168–74.http://dx.doi.org/10.1099/vir.0.051821-010. Kobayashi T, Yanase T, Yamakawa M, Kato T, Yoshida K,Tsuda T. Genetic diversity and reassortments among Akabanevirus field isolates. Virus Res. 2007;130:162–71. http://dx.doi.org/10.1016/j.virusres.2007.06.00711. Bilk S, Schulze C, Fischer M, Beer M, Hlinak A, Hoffmann B.Organ distribution of Schmallenberg virus RNA in malformednewborns. Vet Microbiol. 2012;159:236–8. http://dx.doi.org/10.1016/j.vetmic.2012.03.03512. Wernike K, Eschbaumer M, Schirrmeier H, Blohm U, Breithaupt A,Hoffmann B, et al. Oral exposure, reinfection and cellular immunityto Schmallenberg virus in cattle. Vet Microbiol. 2013;165:155–9.http://dx.doi.org/10.1016/j.vetmic.2013.01.04013. Wernike K, Hoffmann B, Bréard E, Bøtner A, Ponsart C,Zientara S, et al. Schmallenberg virus experimental infection ofsheep. Vet Microbiol. 2013;166:461–6. http://dx.doi.org/10.1016/j.vetmic.2013.06.03014. Méroc E, Poskin A, Van Loo H, Van Driessche E, Czaplicki G,Quinet C, et al. Follow-up of the Schmallenberg virusseroprevalence in Belgian cattle. Transbound Emerg Dis. 2013.http://dx.doi.org/10.1111/tbed.1220215. Wernike K, Elbers A, Beer M. Schmallenberg virus infection.Rev Sci Tech. 2015;34.Address for correspondence: Martin Beer, Friedrich-Loeffler-Institut,Suedufer 10, 17493 Greifswald—Insel Riems, Germany;email: martin.beer@fli.bund.de1204 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 21, No. 7, July 2015
Detection of Circovirus inFoxes with Meningoencephalitis,United Kingdom, 2009–2013Steve Bexton, Lidewij C. Wiersma, Sarah Getu,Peter R. van Run, Georges M.G.M. Verjans,Debby Schipper, Claudia M.E. Schapendonk,Rogier Bodewes, Lucy Oldroyd,Bart L. Haagmans, Marion M.P. Koopmans,Saskia L. SmitsA fox circovirus was identified in serum samples from foxeswith unexplained neurologic signs by using viral metagenomics.Fox circovirus nucleic acid was localized in histologicallesions of the cerebrum by in situ hybridization.Viruses from the family Circoviridae may have neurologictropism more commonly than previously anticipated.Circoviruses (family Circoviridae) are nonenveloped,single-stranded, circular DNA (≈2 kb) viruses (1). Twogenera, Circovirus and Gyrovirus, are recognized, and an additionalgenus, Cyclovirus, has been proposed (1,2). Circoviruseshave an ambisense genome organization with 2 majorinversely arranged open reading frames encoding the rollingcircle replication initiator protein gene (Rep) and a capsidprotein gene (Cap) (1). A conserved stem–loop structure, requiredfor viral replication, is located between the 5′ ends ofthe 2 main open reading frames. Circoviruses are thoughtto exhibit host species specificity and have been detectedin various species, including birds, pigs, and dogs (1,3,4).These viruses have been associated with a variety of diseases,including respiratory and enteric disease, dermatitis, andreproductive problems (1,3–5). Recently, many small circularDNA genomes have been described from different hostsby using different methods, including high-throughput sequencing(6). Here we describe the identification, characterization,and prevalence of a newly discovered fox circovirusthat was present in serum and brain samples from foxes withunexplained meningoencephalitis in the United Kingdom.Author affiliations: RSPCA Norfolk Wildlife Hospital, East Winch,United Kingdom (S. Bexton); Erasmus Medical Center, Rotterdam,the Netherlands (L.C. Wiersma, S. Getu, P.R. van Run,G.M.G.M. Verjans, D. Schipper, C.M.E. Schapendonk,R. Bodewes, B.L. Haagmans, M.M.P. Koopmans, S.L. Smits);Abbey Veterinary Services, Newton Abbot, United Kingdom(L. Oldroyd); National Institute for Public Health and theEnvironment, Bilthoven, the Netherlands (M.M.P. Koopmans)DOI: http://dx.doi.org/10.3201/eid2107.150228The StudyDuring 2009–2013, a total of 31 adult foxes with signs ofa neurologic disorder were brought to the RSPCA NorfolkWildlife Hospital in East Winch, United Kingdom. Thefoxes exhibited abnormal behavior, lack of fear, reducedalertness, aimless wandering, circling, facial muscletwitching, hind limb paresis, and visual abnormalities. Caseswere only detected when free-living foxes became debilitatedand were taken to the wildlife rescue center. Oncein captivity, diseased foxes had good appetite and generallysurvived with no substantial disease progression or death,but they showed no evidence of natural recovery. After afew weeks, the foxes were usually euthanized because theydid not respond to (nonspecific) medical treatment. All procedureswere performed in compliance with relevant lawsand institutional guidelines. Following euthanasia, necropsieswere performed according to standard procedures.Samples were stored in 10% neutral buffered formalinand embedded in paraffin, and 4 μm–thick sections werestained with hematoxylin and eosin and evaluated for thepresence of histologic lesions.All foxes had similar histologic findings consisting ofchronic multifocal or diffuse lymphoplasmacytic meningoencephalitisoriented on the forebrain with a predilection forcortical gray matter (Figure 1; Table 1; online Technical AppendixFigure 1, http://wwwnc.cdc.gov/EID/article/21/7/15-0228-Techapp1.<strong>pdf</strong>). Characteristic histopathologic featureswere nonspecific perivascular cuffing, rod cell proliferation,spongiosis, neuronal necrosis, moderate to severe gliosis,neuronal satellitosis, and neurophagia. Substantial pathologicchanges were restricted to the central nervous system.Histopathologic changes suggested viral, protozoal, microsporidial,immune-mediated, or idiopathic disease. Immunohistochemistryof brain samples was negative for caninedistemper virus, canine adenovirus, Borna disease virus,Toxoplasma gondii, and Neospora canium (data not shown).Serologic test results for canine distemper virus, rabies virus,N. canium, and tickborne encephalitis virus were negative,and Ziehl-Neelsen and Giemsa staining results for microsporidiawere negative. Minor white matter involvement,the duration of animal survival, and the current absence ofdocumented rabies cases in the United Kingdom eliminatedrabies virus as the cause of the neurologic disorder.Serum samples from 6 of the foxes (VS7100001–6)were available for virus discovery studies. To perform theEmerging Infectious Diseases • www.cdc.gov/eid • Vol. 21, No. 7, July 2015 1205
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