FREE SHIPPING over $40
OVER 9000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Home / Equine Research Bank / PLoS One / The bicolored white-toothed shrew Crocidura leucodon (HERMAN...
PloS one2014; 9(4); e93659; doi: 10.1371/journal.pone.0093659

The bicolored white-toothed shrew Crocidura leucodon (HERMANN 1780) is an indigenous host of mammalian Borna disease virus.

Abstract: Borna disease (BD) is a sporadic neurologic disease of horses and sheep caused by mammalian Borna disease virus (BDV). Its unique epidemiological features include: limited occurrence in certain endemic regions of central Europe, yearly varying disease peaks, and a seasonal pattern with higher disease frequencies in spring and a disease nadir in autumn. It is most probably not directly transmitted between horses and sheep. All these features led to the assumption that an indigenous virus reservoir of BDV other than horses and sheep may exist. The search for such a reservoir had been unsuccessful until a few years ago five BDV-infected shrews were found in a BD-endemic area in Switzerland. So far, these data lacked further confirmation. We therefore initiated a study in shrews in endemic areas of Germany. Within five years 107 shrews of five different species were collected. BDV infections were identified in 14 individuals of the species bicolored white-toothed shrew (Crocidura leucodon, HERMANN 1780), all originating from BD-endemic territories. Immunohistological analysis showed widespread distribution of BDV antigen both in the nervous system and in epithelial and mesenchymal tissues without pathological alterations. Large amounts of virus, demonstrated by presence of viral antigen in epithelial cells of the oral cavity and in keratinocytes of the skin, may be a source of infection for natural and spill-over hosts. Genetic analyses reflected a close relationship of the BDV sequences obtained from the shrews with the regional BDV cluster. At one location a high percentage of BDV-positive shrews was identified in four consecutive years, which points towards a self-sustaining infection cycle in bicolored white-toothed shrews. Analyses of behavioral and population features of this shrew species revealed that the bicolored white-toothed shrew may indeed play an important role as an indigenous host of BDV.
Get Full Text
Publication Date: 2014-04-03 PubMed ID: 24699636PubMed Central: PMC3974811DOI: 10.1371/journal.pone.0093659Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
LinkedInCopy
  • Journal Article
  • Research Support
  • Non-U.S. Gov't

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This research focuses on identifying an indigenous virus reservoir for Borna disease virus (BDV), which is a sporadic neurologic disease in horses and sheep. The researchers found that the bicolored white-toothed shrew is likely an important host for BDV, showing evidence of self-sustaining infection cycles and significant amounts of the virus in their systems.

Introduction and Background

  • Borna disease (BD) is a neurologic disease seen in horses and sheep and it is caused by the Borna Disease Virus (BDV).
  • The disease has unique epidemiological features such as limited occurrence in certain endemic regions of central Europe, differing disease peaks yearly, and a distinct seasonal pattern.
  • Historically, it was assumed that this disease was not directly transmitted between horses and sheep and researchers hypothesized that an unidentified indigenous virus reservoir for BDV might exist.

Research Methodology

  • Based on previous findings of BDV-infected shrews in an endemic area in Switzerland, the researchers initiated a study on shrews in BD-endemic areas of Germany for a period of five years.
  • Through their research, they were able to collect 107 shrews of five different species.

Research Findings

  • The researchers identified BDV infections in 14 individuals belonging to the species of bicolored white-toothed shrew, all coming from BD-endemic territories.
  • Immunohistological analysis showed a widespread distribution of BDV antigen in the nervous system of these shrews and in their epithelial and mesenchymal tissues without pathological alterations.
  • High presence of the viral antigen in the shrew’s oral cavity cells and skin keratinocytes suggests that these areas could be potential sources of infection for natural and spill-over hosts.
  • Genetic analyses showed a close relationship between the BDV sequences found in the shrews and the regional BDV cluster, reinforcing their role as a host species.

Conclusions and Implications

  • The study identified consistent BDV infection in bicolored white-toothed shrews over multiple consecutive years at one location, suggesting a self-sustaining infection cycle.
  • The population and behavioral features of the bicolored white-toothed shrew also suggest that it may play an important role as an indigenous host of BDV.
  • With the information from this study, future BD research could target effective interventions and control measures for BD in the indigenous host, potentially reducing disease incidence in horses and sheep.

Cite This Article

APA
Dürrwald R, Kolodziejek J, Weissenböck H, Nowotny N. (2014). The bicolored white-toothed shrew Crocidura leucodon (HERMANN 1780) is an indigenous host of mammalian Borna disease virus. PLoS One, 9(4), e93659. https://doi.org/10.1371/journal.pone.0093659

Publication

PloS one
ISSN: 1932-6203
NlmUniqueID: 101285081
Country: United States
Language: English
Volume: 9
Issue: 4
Pages: e93659
PII: e93659

Researcher Affiliations

Dürrwald, Ralf
  • IDT Biologika GmbH (IDT), Dessau-Roβlau, Germany.
Kolodziejek, Jolanta
  • Viral Zoonoses, Emerging and Vector-Borne Infections Group, Institute of Virology, Department of Pathobiology, University of Veterinary Medicine Vienna, Vienna, Austria.
Weissenböck, Herbert
  • Institute of Pathology and Forensic Veterinary Medicine, Department of Pathobiology, University of Veterinary Medicine Vienna, Vienna, Austria.
Nowotny, Norbert
  • Viral Zoonoses, Emerging and Vector-Borne Infections Group, Institute of Virology, Department of Pathobiology, University of Veterinary Medicine Vienna, Vienna, Austria; Department of Microbiology and Immunology, College of Medicine and Health Sciences, Sultan Qaboos University, Muscat, Oman.

MeSH Terms

  • Animals
  • Base Sequence
  • Borna disease virus / classification
  • Borna disease virus / isolation & purification
  • DNA Primers
  • Disease Vectors
  • Molecular Sequence Data
  • Phylogeny
  • Polymerase Chain Reaction
  • Shrews / virology

Conflict of Interest Statement

RD is employed at IDT Biologika GmbH, Germany. This company had a vaccine on the market against Borna disease for horses and sheep until 1991 but is not dealing with the topic of Borna disease any more. After leaving University RD continued research on the epidemiology of Borna disease in his private time. This does not alter the authors’ adherence to all the PLOS ONE policies on sharing data and materials.

References

This article includes 81 references
  1. Briese T, Schneemann A, Lewis AJ, Park YS, Kim S, Ludwig H, Lipkin WI. Genomic organization of Borna disease virus.. Proc Natl Acad Sci U S A 1994 May 10;91(10):4362-6.
    pmc: PMC43785pubmed: 8183914doi: 10.1073/pnas.91.10.4362google scholar: lookup
  2. Cubitt B, Oldstone C, de la Torre JC. Sequence and genome organization of Borna disease virus.. J Virol 1994 Mar;68(3):1382-96.
    pmc: PMC236592pubmed: 7906311doi: 10.1128/jvi.68.3.1382-1396.1994google scholar: lookup
  3. Schwemmle M, Carbone KM, Tomonago K, Nowotny N, Garten W. Family Bornaviridae. Virus Taxonomy. Eighth Report of the International Committee on Taxonomy of Viruses 2005;615–622.
  4. Staeheli P, Sauder C, Hausmann J, Ehrensperger F, Schwemmle M. Epidemiology of Borna disease virus.. J Gen Virol 2000 Sep;81(Pt 9):2123-2135.
    pubmed: 10950968doi: 10.1099/0022-1317-81-9-2123google scholar: lookup
  5. Kistler AL, Gancz A, Clubb S, Skewes-Cox P, Fischer K, Sorber K, Chiu CY, Lublin A, Mechani S, Farnoushi Y, Greninger A, Wen CC, Karlene SB, Ganem D, DeRisi JL. Recovery of divergent avian bornaviruses from cases of proventricular dilatation disease: identification of a candidate etiologic agent.. Virol J 2008 Jul 31;5:88.
    pmc: PMC2546392pubmed: 18671869doi: 10.1186/1743-422x-5-88google scholar: lookup
  6. Weissenböck H, Bakonyi T, Sekulin K, Ehrensperger F, Doneley RJ, Dürrwald R, Hoop R, Erdélyi K, Gál J, Kolodziejek J, Nowotny N. Avian bornaviruses in psittacine birds from Europe and Australia with proventricular dilatation disease.. Emerg Infect Dis 2009 Sep;15(9):1453-9.
    pmc: PMC2819881pubmed: 19788814doi: 10.3201/eid1509.090353google scholar: lookup
  7. Weissenböck H, Sekulin K, Bakonyi T, Högler S, Nowotny N. Novel avian bornavirus in a nonpsittacine species (Canary; Serinus canaria) with enteric ganglioneuritis and encephalitis.. J Virol 2009 Nov;83(21):11367-71.
    pmc: PMC2772780pubmed: 19706702doi: 10.1128/jvi.01343-09google scholar: lookup
  8. Staeheli P, Rinder M, Kaspers B. Avian bornavirus associated with fatal disease in psittacine birds.. J Virol 2010 Jul;84(13):6269-75.
    pmc: PMC2903261pubmed: 20219910doi: 10.1128/jvi.02567-09google scholar: lookup
  9. Horie M, Honda T, Suzuki Y, Kobayashi Y, Daito T, Oshida T, Ikuta K, Jern P, Gojobori T, Coffin JM, Tomonaga K. Endogenous non-retroviral RNA virus elements in mammalian genomes.. Nature 2010 Jan 7;463(7277):84-7.
    pmc: PMC2818285pubmed: 20054395doi: 10.1038/nature08695google scholar: lookup
  10. Belyi VA, Levine AJ, Skalka AM. Unexpected inheritance: multiple integrations of ancient bornavirus and ebolavirus/marburgvirus sequences in vertebrate genomes.. PLoS Pathog 2010 Jul 29;6(7):e1001030.
    pmc: PMC2912400pubmed: 20686665doi: 10.1371/journal.ppat.1001030google scholar: lookup
  11. Katzourakis A, Gifford RJ. Endogenous viral elements in animal genomes.. PLoS Genet 2010 Nov 18;6(11):e1001191.
    pmc: PMC2987831pubmed: 21124940doi: 10.1371/journal.pgen.1001191google scholar: lookup
  12. Kobayashi Y, Horie M, Tomonaga K, Suzuki Y. No evidence for natural selection on endogenous borna-like nucleoprotein elements after the divergence of Old World and New World monkeys.. PLoS One 2011;6(9):e24403.
    pmc: PMC3166317pubmed: 21912690doi: 10.1371/journal.pone.0024403google scholar: lookup
  13. Hausmann J, Hallensleben W, de la Torre JC, Pagenstecher A, Zimmermann C, Pircher H, Staeheli P. T cell ignorance in mice to Borna disease virus can be overcome by peripheral expression of the viral nucleoprotein.. Proc Natl Acad Sci U S A 1999 Aug 17;96(17):9769-74.
    pmc: PMC22285pubmed: 10449769doi: 10.1073/pnas.96.17.9769google scholar: lookup
  14. Stitz L, Planz O, Bilzer T, Frei K, Fontana A. Transforming growth factor-beta modulates T cell-mediated encephalitis caused by Borna disease virus. Pathogenic importance of CD8+ cells and suppression of antibody formation.. J Immunol 1991 Nov 15;147(10):3581-6.
    pubmed: 1940357
  15. Zwick W. Bornasche Krankheit und Enzephalomyelitis der Tiere. Handbuch der Viruskrankheiten II 1939;254–354.
  16. Authenrieth CF. Ueber die hitzige Kopf-Krankheit der Pferde. 1823;47 p. Supplement 19 p..
  17. Dürrwald R, Ludwig H. Borna disease virus (BDV), a (zoonotic?) worldwide pathogen. A review of the history of the disease and the virus infection with comprehensive bibliography.. Zentralbl Veterinarmed B 1997 May;44(3):147-84.
    pubmed: 9197210doi: 10.1111/j.1439-0450.1997.tb00962.xgoogle scholar: lookup
  18. Joest E, Degen K. Untersuchungen über die pathologische Histologie, Pathogenese und postmortale Diagnose der seuchenhaften Gehirn-Rückenmarksentzündung (Bornaschen Krankheit) des Pferdes. Zeitschr Infektionskrankh parasit Krankh Hyg Haustiere 1911;9:1–98.
  19. Dürrwald R, Kolodziejek J, Muluneh A, Herzog S, Nowotny N. Epidemiological pattern of classical Borna disease and regional genetic clustering of Borna disease viruses point towards the existence of to-date unknown endemic reservoir host populations.. Microbes Infect 2006 Mar;8(3):917-29.
    pubmed: 16469519doi: 10.1016/j.micinf.2005.08.013google scholar: lookup
  20. Nowotny N, Kolodziejek J, Jehle CO, Suchy A, Staeheli P, Schwemmle M. Isolation and characterization of a new subtype of Borna disease virus.. J Virol 2000 Jun;74(12):5655-8.
    pmc: PMC112053pubmed: 10823873doi: 10.1128/jvi.74.12.5655-5658.2000google scholar: lookup
  21. Pleschka S, Staeheli P, Kolodziejek J, Richt JA, Nowotny N, Schwemmle M. Conservation of coding potential and terminal sequences in four different isolates of Borna disease virus.. J Gen Virol 2001 Nov;82(Pt 11):2681-2690.
    pubmed: 11602780doi: 10.1099/0022-1317-82-11-2681google scholar: lookup
  22. Weissenböck H, Nowotny N, Caplazi P, Kolodziejek J, Ehrensperger F. Borna disease in a dog with lethal meningoencephalitis.. J Clin Microbiol 1998 Jul;36(7):2127-30.
    pmc: PMC105002pubmed: 9650982doi: 10.1128/jcm.36.7.2127-2130.1998google scholar: lookup
  23. Schwemmle M, Jehle C, Formella S, Staeheli P. Sequence similarities between human bornavirus isolates and laboratory strains question human origin.. Lancet 1999 Dec 4;354(9194):1973-4.
    pubmed: 10622306doi: 10.1016/s0140-6736(99)04703-0google scholar: lookup
  24. Dürrwald R, Kolodziejek J, Herzog S, Nowotny N. Meta-analysis of putative human bornavirus sequences fails to provide evidence implicating Borna disease virus in mental illness.. Rev Med Virol 2007 May-Jun;17(3):181-203.
    pubmed: 17342788doi: 10.1002/rmv.530google scholar: lookup
  25. Hornig M, Briese T, Licinio J, Khabbaz RF, Altshuler LL, Potkin SG, Schwemmle M, Siemetzki U, Mintz J, Honkavuori K, Kraemer HC, Egan MF, Whybrow PC, Bunney WE, Lipkin WI. Absence of evidence for bornavirus infection in schizophrenia, bipolar disorder and major depressive disorder.. Mol Psychiatry 2012 May;17(5):486-93.
    pmc: PMC3622588pubmed: 22290118doi: 10.1038/mp.2011.179google scholar: lookup
  26. Bode L, Riegel S, Lange W, Ludwig H. Human infections with Borna disease virus: seroprevalence in patients with chronic diseases and healthy individuals.. J Med Virol 1992 Apr;36(4):309-15.
    pubmed: 1578223doi: 10.1002/jmv.1890360414google scholar: lookup
  27. Güngör S, Anlar B, Turan N, Yilmaz H, Helps CR, Harbour DA. Antibodies to borna disease virus in subacute sclerosing panencephalitis.. Pediatr Infect Dis J 2005 Sep;24(9):833-4.
    pubmed: 16148853doi: 10.1097/01.inf.0000178307.70429.75google scholar: lookup
  28. Dürrwald R. Die natürliche Borna-Virus-Infektion der Einhufer und Schafe. Untersuchungen zur Epidemiologie, zu neueren diagnostischen Methoden (ELISA, PCR) und zur Antikörperkinetik bei Pferden nach Vakzination mit Lebendimpfstoff. 1993.
  29. Netzer F. Vorkommen, Verbreitung, Ätiologie und Klinik der Bornaschen Krankheit im Landkreis Pfaffenhofen a. d. Ilm in den Jahren 1950–1952. 1952.
  30. Gosztonyi G, Ludwig H. Borna disease--neuropathology and pathogenesis.. Curr Top Microbiol Immunol 1995;190:39-73.
    pubmed: 7789150
  31. Pletnikov MV, Gonzalez-Dunia D, Stitz L. Experimental infection: Pathogenesis of neurobehavioral disease. Borna disease virus and its role in neurobehavioral disease 2002;125–178.
  32. Sauder C, Staeheli P. Rat model of borna disease virus transmission: epidemiological implications.. J Virol 2003 Dec;77(23):12886-90.
    pmc: PMC262589pubmed: 14610210doi: 10.1128/jvi.77.23.12886-12890.2003google scholar: lookup
  33. Ihlenburg H. Zur Epidemiologie, Diagnose und Behandlung der Bornaschen Krankheit. Arch Exp Veterinarmed 1957;11:635–861.
  34. Vahlenkamp TW, Konrath A, Weber M, Müller H. Persistence of Borna disease virus in naturally infected sheep.. J Virol 2002 Oct;76(19):9735-43.
    pmc: PMC136490pubmed: 12208952doi: 10.1128/jvi.76.19.9735-9743.2002google scholar: lookup
  35. Hilbe M, Herrsche R, Kolodziejek J, Nowotny N, Zlinszky K, Ehrensperger F. Shrews as reservoir hosts of borna disease virus.. Emerg Infect Dis 2006 Apr;12(4):675-7.
    pmc: PMC3294707pubmed: 16704819doi: 10.3201/eid1204.051418google scholar: lookup
  36. Puorger ME, Hilbe M, Müller JP, Kolodziejek J, Nowotny N, Zlinszky K, Ehrensperger F. Distribution of Borna disease virus antigen and RNA in tissues of naturally infected bicolored white-toothed shrews, Crocidura leucodon, supporting their role as reservoir host species.. Vet Pathol 2010 Mar;47(2):236-44.
    pubmed: 20133953doi: 10.1177/0300985809351849google scholar: lookup
  37. Sorg I, Metzler A. Detection of Borna disease virus RNA in formalin-fixed, paraffin-embedded brain tissues by nested PCR.. J Clin Microbiol 1995 Apr;33(4):821-3.
    pmc: PMC228048pubmed: 7790444doi: 10.1128/jcm.33.4.821-823.1995google scholar: lookup
  38. Schneider PA, Briese T, Zimmermann W, Ludwig H, Lipkin WI. Sequence conservation in field and experimental isolates of Borna disease virus.. J Virol 1994 Jan;68(1):63-8.
    pmc: PMC236264pubmed: 8254777doi: 10.1128/jvi.68.1.63-68.1994google scholar: lookup
  39. Bourg M, Herzog S, Encarnação JA, Nobach D, Lange-Herbst H, Eickmann M, Herden C. Bicolored white-toothed shrews as reservoir for borna disease virus, Bavaria, Germany.. Emerg Infect Dis 2013 Dec;19(12):2064-6.
    pmc: PMC3840852pubmed: 24274262doi: 10.3201/eid1912.131076google scholar: lookup
  40. Kinnunen PM, Billich C, Ek-Kommonen C, Henttonen H, Kallio RK, Niemimaa J, Palva A, Staeheli P, Vaheri A, Vapalahti O. Serological evidence for Borna disease virus infection in humans, wild rodents and other vertebrates in Finland.. J Clin Virol 2007 Jan;38(1):64-9.
    pubmed: 17129759doi: 10.1016/j.jcv.2006.10.003google scholar: lookup
  41. Herzog S, Kompter C, Frese K, Rott R. Replication of Borna disease virus in rats: age-dependent differences in tissue distribution.. Med Microbiol Immunol 1984;173(4):171-7.
    pubmed: 6439986doi: 10.1007/bf02122108google scholar: lookup
  42. Herzog S, Frese K, Rott R. Studies on the genetic control of resistance of black hooded rats to Borna disease.. J Gen Virol 1991 Mar;72 ( Pt 3):535-40.
    pubmed: 2005432doi: 10.1099/0022-1317-72-3-535google scholar: lookup
  43. Stitz L, Schilken D, Frese K. Atypical dissemination of the highly neurotropic Borna disease virus during persistent infection in cyclosporine A-treated, immunosuppressed rats.. J Virol 1991 Jan;65(1):457-60.
    pmc: PMC240537pubmed: 1985209doi: 10.1128/jvi.65.1.457-460.1991google scholar: lookup
  44. Stitz L, Nöske K, Planz O, Furrer E, Lipkin WI, Bilzer T. A functional role for neutralizing antibodies in Borna disease: influence on virus tropism outside the central nervous system.. J Virol 1998 Nov;72(11):8884-92.
    pmc: PMC110305pubmed: 9765433doi: 10.1128/jvi.72.11.8884-8892.1998google scholar: lookup
  45. Weissenböck H, Hornig M, Hickey WF, Lipkin WI. Microglial activation and neuronal apoptosis in Bornavirus infected neonatal Lewis rats.. Brain Pathol 2000 Apr;10(2):260-72.
    pmc: PMC8098497pubmed: 10764045doi: 10.1111/j.1750-3639.2000.tb00259.xgoogle scholar: lookup
  46. Okamoto M, Hagiwara K, Kamitani W, Sako T, Hirayama K, Kirisawa R, Tsuji M, Ishihara C, Iwai H, Kobayashi T, Tomonaga K, Ikuta K, Taniyama H. Experimental vertical transmission of Borna disease virus in the mouse.. Arch Virol 2003 Aug;148(8):1557-68.
    pubmed: 12898331doi: 10.1007/s00705-003-0120-ygoogle scholar: lookup
  47. Corbet G, Ovenden D. The mammals of Britain and Europe. 1980;247 p..
  48. Zimmermann G. Ein Beitrag zur Epizootiologie der Borna’schen Krankheit in den Jahren 1948 bis 1952 in Bayern. 1953.
  49. Richter H. Zur Verbreitung der Wimperspitzmäuse (Crocidura, Wagler, 1832) in Mitteleuropa. Abhandlungen und Berichte aus dem Staatl Museum für Tierkunde in Dresden 1963;26:219–242.
  50. Martens JM, Gillandt L. Zum Vorkommen der Feldspitzmaus Crocidura leucodon in Nordost-Niedersachsen 1978/79. Z Säugetierk 1980;45:188–191.
  51. Weber B. Zur nördlichen Verbreitungsgrenze der Feldspitzmaus (Crocidura leucodon) auf dem Gebiet der DDR. Säugetierkd Inf 1983;2:69–73.
  52. Herter K, Thenius E. Die Insektenesser. Grzimeks Tierleben. Enzyklopädie des Tierreiches. Band Säugetiere 1 1977;169–232.
  53. Kraft R. Ehemalige und aktuelle Verbreitung von Hausspitzmaus, Crocidura russula (Hermann, 1780), und Gartenspitzmaus, Crocidura suaveolens (Pallas, 1811), in Bayern. Bonn zool Beitr 2000;49:115–129.
  54. Kraft R. Mäuse und Spitzmäuse in Bayern: Verbreitung, Lebensraum, Bestandssituation. 2008.
  55. Reichelt U. Epizootiologische Untersuchungen zur Bornaschen Krankheit bei Pferden in Bayern und Darstellung des monoklonalen Antikörpers 38/15H7. 2009.
  56. Encarnação JA, Herzog S, Eickmann M, Becker NI, Hermes N, Herden C. Landscape features and reservoir occurrence affecting the risk for equine infection with Borna disease virus.. J Wildl Dis 2013 Oct;49(4):860-8.
    pubmed: 24502713doi: 10.7589/2012-10-262google scholar: lookup
  57. Holmes EC, Woelk CH, Kassis R, Bourhy H. Genetic constraints and the adaptive evolution of rabies virus in nature.. Virology 2002 Jan 20;292(2):247-57.
    pubmed: 11878928doi: 10.1006/viro.2001.1271google scholar: lookup
  58. Weaver SC, Brault AC, Kang W, Holland JJ. Genetic and fitness changes accompanying adaptation of an arbovirus to vertebrate and invertebrate cells.. J Virol 1999 May;73(5):4316-26.
    pmc: PMC104213pubmed: 10196330doi: 10.1128/jvi.73.5.4316-4326.1999google scholar: lookup
  59. Weaver SC, Rico-Hesse R, Scott TW. Genetic diversity and slow rates of evolution in New World alphaviruses.. Curr Top Microbiol Immunol 1992;176:99-117.
    pubmed: 1318187doi: 10.1007/978-3-642-77011-1_7google scholar: lookup
  60. Berg M, Johansson M, Montell H, Berg AL. Wild birds as a possible natural reservoir of Borna disease virus.. Epidemiol Infect 2001 Aug;127(1):173-8.
    pmc: PMC2869725pubmed: 11561971doi: 10.1017/s0950268801005702google scholar: lookup
  61. Kolodziejek J, Dürrwald R, Herzog S, Ehrensperger F, Lussy H, Nowotny N. Genetic clustering of Borna disease virus natural animal isolates, laboratory and vaccine strains strongly reflects their regional geographical origin.. J Gen Virol 2005 Feb;86(Pt 2):385-398.
    pubmed: 15659758doi: 10.1099/vir.0.80587-0google scholar: lookup
  62. MacPhee RDE, Novacek MJ. Definition and relationships of Lipotyphyla. Mammal phylogeny: placentals 1993;13–31.
  63. Cantoni D, Vogel P. Social organization and mating systems of free-ranging greater white-toothed shrews, Crocidura russula. Anim Behav 1989;38:205–214.
  64. Favre L, Balloux F, Goudet J, Perrin N. Female-biased dispersal in the monogamous mammal Crocidura russula: evidence from field data and microsatellite patterns.. Proc Biol Sci 1997 Jan 22;264(1378):127-32.
    pmc: PMC1688234pubmed: 9061966doi: 10.1098/rspb.1997.0019google scholar: lookup
  65. Duarte LC, Bouteiller C, Fontanillas IP, Petit E, Perrin N. Inbreeding in the greater white-toothed shrew, Crocidura russula.. Evolution 2003 Mar;57(3):638-45.
    pubmed: 12703953doi: 10.1111/j.0014-3820.2003.tb01555.xgoogle scholar: lookup
  66. Balloux F, Goudet J, Perrin N. BREEDING SYSTEM AND GENETIC VARIANCE IN THE MONOGAMOUS, SEMI-SOCIAL SHREW, CROCIDURA RUSSULA.. Evolution 1998 Aug;52(4):1230-1235.
    pubmed: 28565220doi: 10.1111/j.1558-5646.1998.tb01851.xgoogle scholar: lookup
  67. Schüppel K-F, Kinne J, Reinacher M. Bornavirus-Antigennachweis bei Alpakas (Lama pacos) sowie bei einem Faultier (Choloepus didactylus) und einem Zwergflusspferd (Choeropsis liberiensis). Verhandlungsbericht XXXVI. Internationales Symposium über Erkrankungen von Zootieren, Kristiansund, Norway 1994;11–15.
  68. Katz JB, Alstad D, Jenny AL, Carbone KM, Rubin SA, Waltrip RW 2nd. Clinical, serologic, and histopathologic characterization of experimental Borna disease in ponies.. J Vet Diagn Invest 1998 Oct;10(4):338-43.
    pubmed: 9786521doi: 10.1177/104063879801000405google scholar: lookup
  69. Jacobsen B, Algermissen D, Schaudien D, Venner M, Herzog S, Wentz E, Hewicker-Trautwein M, Baumgärtner W, Herden C. Borna disease in an adult alpaca stallion (Lama pacos).. J Comp Pathol 2010 Aug-Oct;143(2-3):203-8.
    pubmed: 20153871doi: 10.1016/j.jcpa.2010.01.009google scholar: lookup
  70. Priestnall SL, Schöniger S, Ivens PA, Eickmann M, Brachthäuser L, Kehr K, Tupper C, Piercy RJ, Menzies-Gow NJ, Herden C. Borna disease virus infection of a horse in Great Britain.. Vet Rec 2011 Apr 9;168(14):380b.
    pubmed: 21498268doi: 10.1136/vr.c6405google scholar: lookup
  71. Kinnunen PM, Inkeroinen H, Ilander M, Kallio ER, Heikkilä HP, Koskela E, Mappes T, Palva A, Vaheri A, Kipar A, Vapalahti O. Intracerebral Borna disease virus infection of bank voles leading to peripheral spread and reverse transcription of viral RNA.. PLoS One 2011;6(8):e23622.
    pmc: PMC3174072pubmed: 21935357doi: 10.1371/journal.pone.0023622google scholar: lookup
  72. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods.. Mol Biol Evol 2011 Oct;28(10):2731-9.
    pmc: PMC3203626pubmed: 21546353doi: 10.1093/molbev/msr121google scholar: lookup
  73. Chvala S, Kolodziejek J, Nowotny N, Weissenböck H. Pathology and viral distribution in fatal Usutu virus infections of birds from the 2001 and 2002 outbreaks in Austria.. J Comp Pathol 2004 Aug-Oct;131(2-3):176-85.
    pubmed: 15276857doi: 10.1016/j.jcpa.2004.03.004google scholar: lookup
  74. Billich C, Sauder C, Frank R, Herzog S, Bechter K, Takahashi K, Peters H, Staeheli P, Schwemmle M. High-avidity human serum antibodies recognizing linear epitopes of Borna disease virus proteins.. Biol Psychiatry 2002 Jun 15;51(12):979-87.
    pubmed: 12062882doi: 10.1016/s0006-3223(02)01387-2google scholar: lookup
  75. Leistner E. Epizootische Betrachtungen über die Encephalomyelitis enzootica equi (Bornasche Krankheit) im rechtsrheinischen Bayern. 1948.
  76. Düwel D. Seuchenkarte der Bornaschen Krankheit. 1957.
  77. Karasek E. Die Verbreitung der Bornaschen Krankheit in Thüringen. Monatsh Veterinärmed 1963;18:868–876.
  78. Metzler A, Frei U, Danner K. [Virologically confirmed outbreak of Borna's disease in a Swiss herd of sheep].. Schweiz Arch Tierheilkd 1976 Nov;118(11):483-92.
    pubmed: 1006278
  79. Caplazi P, Melzer K, Goetzmann R, Rohner-Cotti A, Bracher V, Zlinszky K, Ehrensperger F. [Borna disease in Switzerland and in the principality of Liechtenstein].. Schweiz Arch Tierheilkd 1999;141(11):521-7.
    pubmed: 10596273
  80. Suchy A, Weissenböck H, Caplazi P, Herzog S, Nowotny N. Equine Borna disease in Austria: evidence for a new endemic area of the natural disease. Equine Pract 2000;22:26–27.
  81. Weissenböck H, Suchy A, Caplazi P, Herzog S, Nowotny N. Borna disease in Austrian horses.. Vet Rec 1998 Jul 4;143(1):21-2.
    pubmed: 9698629doi: 10.1136/vr.143.1.21google scholar: lookup

Citations

This article has been cited 30 times.
  1. Weiss V, Weidinger P, Matt J, Weissenbacher-Lang C, Nowotny N, Weissenböck H. Rustrela Virus-Associated Encephalomyelitis ('Staggering Disease') in Cats from Eastern Austria, 1994-2016.. Viruses 2023 Jul 25;15(8).
    doi: 10.3390/v15081621pubmed: 37631964google scholar: lookup
  2. Ulrich RG, Drewes S, Haring V, Panajotov J, Pfeffer M, Rubbenstroth D, Dreesman J, Beer M, Dobler G, Knauf S, Johne R, Böhmer MM. [Viral zoonoses in Germany: a One Health perspective].. Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz 2023 Jun;66(6):599-616.
    doi: 10.1007/s00103-023-03709-0pubmed: 37261460google scholar: lookup
  3. Allartz P, Hotop SK, Muntau B, Schlaphof A, Thomé-Bolduan C, Gabriel M, Petersen N, Lintzel M, Behrens C, Eggert P, Pörtner K, Steiner J, Brönstrup M, Tappe D. Detection of bornavirus-reactive antibodies and BoDV-1 RNA only in encephalitis patients from virus endemic areas: a comparative serological and molecular sensitivity, specificity, predictive value, and disease duration correlation study.. Infection 2023 May 30;:1-13.
    doi: 10.1007/s15010-023-02048-1pubmed: 37253816google scholar: lookup
  4. Grosse L, Lieftüchter V, Vollmuth Y, Hoffmann F, Olivieri M, Reiter K, Tacke M, Heinen F, Borggraefe I, Osterman A, Forstner M, Hübner J, von Both U, Birzele L, Rohlfs M, Schomburg A, Böhmer MM, Ruf V, Cadar D, Muntau B, Pörtner K, Tappe D. First detected geographical cluster of BoDV-1 encephalitis from same small village in two children: therapeutic considerations and epidemiological implications.. Infection 2023 Feb 23;:1-16.
    doi: 10.1007/s15010-023-01998-wpubmed: 36821024google scholar: lookup
  5. Huhndorf M, Juhasz J, Wattjes MP, Schilling A, Schob S, Kaden I, Klaß G, Tappe D. Magnetic resonance imaging of human variegated squirrel bornavirus 1 (VSBV-1) encephalitis reveals diagnostic pattern indistinguishable from Borna disease virus 1 (BoDV-1) encephalitis but typical for bornaviruses.. Emerg Microbes Infect 2023 Dec;12(1):2179348.
    doi: 10.1080/22221751.2023.2179348pubmed: 36757188google scholar: lookup
  6. Pörtner K, Wilking H, Frank C, Böhmer MM, Stark K, Tappe D. Risk factors for Borna disease virus 1 encephalitis in Germany - a case-control study.. Emerg Microbes Infect 2023 Dec;12(1):e2174778.
    doi: 10.1080/22221751.2023.2174778pubmed: 36748319google scholar: lookup
  7. Eidenschink L, Knoll G, Tappe D, Offner R, Drasch T, Ehrl Y, Banas B, Banas MC, Niller HH, Gessner A, Köstler J, Lampl BMJ, Pregler M, Völkl M, Kunkel J, Neumann B, Angstwurm K, Schmidt B, Bauswein M. IFN-γ-Based ELISpot as a New Tool to Detect Human Infections with Borna Disease Virus 1 (BoDV-1): A Pilot Study.. Viruses 2023 Jan 10;15(1).
    doi: 10.3390/v15010194pubmed: 36680234google scholar: lookup
  8. Bauswein M, Eidenschink L, Knoll G, Neumann B, Angstwurm K, Zoubaa S, Riemenschneider MJ, Lampl BMJ, Pregler M, Niller HH, Jantsch J, Gessner A, Eberhardt Y, Huppertz G, Schramm T, Kühn S, Koller M, Drasch T, Ehrl Y, Banas B, Offner R, Schmidt B, Banas MC. Human Infections with Borna Disease Virus 1 (BoDV-1) Primarily Lead to Severe Encephalitis: Further Evidence from the Seroepidemiological BoSOT Study in an Endemic Region in Southern Germany.. Viruses 2023 Jan 9;15(1).
    doi: 10.3390/v15010188pubmed: 36680228google scholar: lookup
  9. Dürrwald R, Kolodziejek J, Oh DY, Herzog S, Liebermann H, Osterrieder N, Nowotny N. Vaccination against Borna Disease: Overview, Vaccine Virus Characterization and Investigation of Live and Inactivated Vaccines.. Viruses 2022 Dec 2;14(12).
    doi: 10.3390/v14122706pubmed: 36560710google scholar: lookup
  10. Rubbenstroth D. Avian Bornavirus Research-A Comprehensive Review.. Viruses 2022 Jul 11;14(7).
    doi: 10.3390/v14071513pubmed: 35891493google scholar: lookup
  11. Rauch J, Steffen JF, Muntau B, Gisbrecht J, Pörtner K, Herden C, Niller HH, Bauswein M, Rubbenstroth D, Mehlhoop U, Allartz P, Tappe D. Human Borna disease virus 1 encephalitis shows marked pro-inflammatory biomarker and tissue immunoactivation during the course of disease.. Emerg Microbes Infect 2022 Dec;11(1):1843-1856.
    doi: 10.1080/22221751.2022.2098831pubmed: 35788177google scholar: lookup
  12. Reinmiedl J, Schulz H, Ruf VC, Hernandez Petzsche MR, Rissland J, Tappe D. Healthcare-associated exposure to Borna disease virus 1 (BoDV-1).. J Occup Med Toxicol 2022 Jun 9;17(1):13.
    doi: 10.1186/s12995-022-00353-3pubmed: 35681207google scholar: lookup
  13. Neumann B, Angstwurm K, Linker RA, Knoll G, Eidenschink L, Rubbenstroth D, Schlottau K, Beer M, Schreiner P, Soutschek E, Böhmer MM, Lampl BMJ, Pregler M, Scheiter A, Evert K, Zoubaa S, Riemenschneider MJ, Asbach B, Gessner A, Niller HH, Schmidt B, Bauswein M. Antibodies against viral nucleo-, phospho-, and X protein contribute to serological diagnosis of fatal Borna disease virus 1 infections.. Cell Rep Med 2022 Jan 18;3(1):100499.
    doi: 10.1016/j.xcrm.2021.100499pubmed: 35106511google scholar: lookup
  14. Frank C, Wickel J, Brämer D, Matschke J, Ibe R, Gazivoda C, Günther A, Hartmann C, Rehn K, Cadar D, Mayer TE, Pörtner K, Wilking H, Schmidt-Chanasit J, Tappe D. Human Borna disease virus 1 (BoDV-1) encephalitis cases in the north and east of Germany.. Emerg Microbes Infect 2022 Dec;11(1):6-13.
    doi: 10.1080/22221751.2021.2007737pubmed: 34783638google scholar: lookup
  15. Kanda T, Horie M, Komatsu Y, Tomonaga K. The Borna Disease Virus 2 (BoDV-2) Nucleoprotein Is a Conspecific Protein That Enhances BoDV-1 RNA-Dependent RNA Polymerase Activity.. J Virol 2021 Oct 13;95(21):e0093621.
    doi: 10.1128/JVI.00936-21pubmed: 34406860google scholar: lookup
  16. Tappe D, Pörtner K, Frank C, Wilking H, Ebinger A, Herden C, Schulze C, Muntau B, Eggert P, Allartz P, Schuldt G, Schmidt-Chanasit J, Beer M, Rubbenstroth D. Investigation of fatal human Borna disease virus 1 encephalitis outside the previously known area for human cases, Brandenburg, Germany - a case report.. BMC Infect Dis 2021 Aug 10;21(1):787.
    doi: 10.1186/s12879-021-06439-3pubmed: 34376142google scholar: lookup
  17. Eisermann P, Rubbenstroth D, Cadar D, Thomé-Bolduan C, Eggert P, Schlaphof A, Leypoldt F, Stangel M, Fortwängler T, Hoffmann F, Osterman A, Zange S, Niller HH, Angstwurm K, Pörtner K, Frank C, Wilking H, Beer M, Schmidt-Chanasit J, Tappe D. Active Case Finding of Current Bornavirus Infections in Human Encephalitis Cases of Unknown Etiology, Germany, 2018-2020.. Emerg Infect Dis 2021 May;27(5):1371-1379.
    doi: 10.3201/eid2705.204490pubmed: 33900167google scholar: lookup
  18. More S, Bøtner A, Butterworth A, Calistri P, Depner K, Edwards S, Garin-Bastuji B, Good M, Gortázar Schmidt C, Michel V, Miranda MA, Nielsen SS, Raj M, Sihvonen L, Spoolder H, Stegeman JA, Thulke HH, Velarde A, Willeberg P, Winckler C, Baldinelli F, Broglia A, Dhollander S, Beltrán-Beck B, Kohnle L, Bicout D. Assessment of listing and categorisation of animal diseases within the framework of the Animal Health Law (Regulation (EU) No 2016/429): Borna disease.. EFSA J 2017 Jul;15(7):e04951.
    doi: 10.2903/j.efsa.2017.4951pubmed: 32625602google scholar: lookup
  19. Tappe D, Frank C, Offergeld R, Wagner-Wiening C, Stark K, Rubbenstroth D, Giese S, Lattwein E, Schwemmle M, Beer M, Schmidt-Chanasit J, Wilking H. Low prevalence of Borna disease virus 1 (BoDV-1) IgG antibodies in humans from areas endemic for animal Borna disease of Southern Germany.. Sci Rep 2019 Dec 27;9(1):20154.
    doi: 10.1038/s41598-019-56839-4pubmed: 31882942google scholar: lookup
  20. Petzold J, van den Brand JMA, Nobach D, Hoffmann B, Hoffmann D, Fast C, Reusken CBEM, van Run PRWA, Schlottau K, Beer M, Herden C. Distribution of zoonotic variegated squirrel bornavirus 1 in naturally infected variegated and Prevost's squirrels.. Sci Rep 2019 Aug 6;9(1):11402.
    doi: 10.1038/s41598-019-47767-4pubmed: 31388038google scholar: lookup
  21. Liesche F, Ruf V, Zoubaa S, Kaletka G, Rosati M, Rubbenstroth D, Herden C, Goehring L, Wunderlich S, Wachter MF, Rieder G, Lichtmannegger I, Permanetter W, Heckmann JG, Angstwurm K, Neumann B, Märkl B, Haschka S, Niller HH, Schmidt B, Jantsch J, Brochhausen C, Schlottau K, Ebinger A, Hemmer B, Riemenschneider MJ, Herms J, Beer M, Matiasek K, Schlegel J. The neuropathology of fatal encephalomyelitis in human Borna virus infection.. Acta Neuropathol 2019 Oct;138(4):653-665.
    doi: 10.1007/s00401-019-02047-3pubmed: 31346692google scholar: lookup
  22. . Bornavirus : Stellungnahmen des Arbeitskreises Blut des Bundesministeriums für Gesundheit.. Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz 2019 Apr;62(4):519-532.
    doi: 10.1007/s00103-019-02904-2pubmed: 30820613google scholar: lookup
  23. Schmutzhard E, Pfausler B. [Rabies and Bornavirus encephalitis : Fatal emerging viral encephalitis-a potential problem for organ recipients].. Nervenarzt 2018 Dec;89(12):1332-1337.
    doi: 10.1007/s00115-018-0620-3pubmed: 30276429google scholar: lookup
  24. Weissenböck H, Bagó Z, Kolodziejek J, Hager B, Palmetzhofer G, Dürrwald R, Nowotny N. Infections of horses and shrews with Bornaviruses in Upper Austria: a novel endemic area of Borna disease.. Emerg Microbes Infect 2017 Jun 21;6(6):e52.
    doi: 10.1038/emi.2017.36pubmed: 28634359google scholar: lookup
  25. Schlottau K, Jenckel M, van den Brand J, Fast C, Herden C, Höper D, Homeier-Bachmann T, Thielebein J, Mensing N, Diender B, Hoffmann D, Ulrich RG, Mettenleiter TC, Koopmans M, Tappe D, Schmidt-Chanasit J, Reusken CB, Beer M, Hoffmann B. Variegated Squirrel Bornavirus 1 in Squirrels, Germany and the Netherlands.. Emerg Infect Dis 2017 Mar;23(3):477-481.
    doi: 10.3201/eid2303.161061pubmed: 28221112google scholar: lookup
  26. Bourg M, Nobach D, Herzog S, Lange-Herbst H, Nesseler A, Hamann HP, Becker S, Höper D, Hoffmann B, Eickmann M, Herden C. Screening red foxes (Vulpes vulpes) for possible viral causes of encephalitis.. Virol J 2016 Sep 2;13(1):151.
    doi: 10.1186/s12985-016-0608-1pubmed: 27590473google scholar: lookup
  27. Rubbenstroth D, Schmidt V, Rinder M, Legler M, Twietmeyer S, Schwemmer P, Corman VM. Phylogenetic Analysis Supports Horizontal Transmission as a Driving Force of the Spread of Avian Bornaviruses.. PLoS One 2016;11(8):e0160936.
    doi: 10.1371/journal.pone.0160936pubmed: 27537693google scholar: lookup
  28. Nobach D, Bourg M, Herzog S, Lange-Herbst H, Encarnação JA, Eickmann M, Herden C. Shedding of Infectious Borna Disease Virus-1 in Living Bicolored White-Toothed Shrews.. PLoS One 2015;10(8):e0137018.
    doi: 10.1371/journal.pone.0137018pubmed: 26313904google scholar: lookup
  29. Kuhn JH, Dürrwald R, Bào Y, Briese T, Carbone K, Clawson AN, deRisi JL, Garten W, Jahrling PB, Kolodziejek J, Rubbenstroth D, Schwemmle M, Stenglein M, Tomonaga K, Weissenböck H, Nowotny N. Taxonomic reorganization of the family Bornaviridae.. Arch Virol 2015 Feb;160(2):621-32.
    doi: 10.1007/s00705-014-2276-zpubmed: 25449305google scholar: lookup
  30. Guo J, Shivaprasad HL, Rech RR, Heatley JJ, Tizard I, Payne S. Characterization of a new genotype of avian bornavirus from wild ducks.. Virol J 2014 Nov 19;11:197.
    doi: 10.1186/s12985-014-0197-9pubmed: 25408146google scholar: lookup
Subscribe to our newsletter
Join 99,344 horse owners like you who receive our email updates on horse health and nutrition.