Abstract
The recently discovered variegated squirrel bornavirus 1 (VSBV-1) caused the death of three squirrel breeders in Germany. Subsequent first screening of squirrels with in vivo collected swab samples and a VSBV-1-specific RT-qPCR revealed not only variegated squirrel infections (Sciurus variegatoides), but also Prevost’s squirrels (Callosciurus prevostii) as positive for VSBV-1 genome. In this study, 328 squirrels were tested using the established RT-qPCR assays. In 16 individual animals VSBV-1 RNA could be detected; 15 individuals were from small breedings and zoological gardens in Germany, with the remaining individual being from a zoological garden in Croatia. Positive animals belonged to the species C. prevostii, C. finlaysonii, and Tamiops swinhoei within the subfamily Callosciurinae and Sciurus granatensis within the subfamily Sciurinae. Repeated non-invasive oral swab sampling in one holding indicated positive animals months after a first negative result. Besides the oral swabs, VSBV-1 was also detected in fecal (pool) samples allowing the future monitoring of squirrel holdings based on RT-qPCR investigation of such samples. The detection in zoological gardens emphasizes the need for further investigations into the transmission route to humans in order to develop rational public health measures for prevention of transmission. Finally, the detection of several closely related VSBV-1 sequences in squirrels from different subfamilies raises questions as to the origin of the virus.
Similar content being viewed by others
References
Briese T, Schneemann A, Lewis AJ, Park YS, Kim S, Ludwig H et al (1994) Genomic organization of Borna disease virus. Proc Natl Acad Sci USA 91(10):4362–4366
Kuhn JH, Durrwald R, Bao Y, Briese T, Carbone K, Clawson AN et al (2015) Taxonomic reorganization of the family Bornaviridae. Arch Virol 160(2):621–632
Hoffmann B, Tappe D, Hoper D, Herden C, Boldt A, Mawrin C et al (2015) A Variegated squirrel bornavirus associated with fatal human encephalitis. N Engl J Med 373(2):154–162
Schlottau K, Jenckel M, van den Brand J, Fast C, Herden C, Höper D et al (2017) Variegated squirrel bornavirus 1 in squirrels, Germany and the Netherlands. Emerg Infect Dis J 23(3):477–481
Wilson DE, Reeder DM (2005) Mammal species of the world: a taxonomic and geographic reference, 3rd edn. John Hopkins University Press, Baltimore, pp 757–789
Bourg M, Herzog S, Encarnacao JA, Nobach D, Lange-Herbst H, Eickmann M et al (2013) Bicolored white-toothed shrews as reservoir for borna disease virus, Bavaria, Germany. Emerg Infect Dis 19(12):2064–2066
Durrwald R, Kolodziejek J, Weissenbock 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
Hilbe M, Herrsche R, Kolodziejek J, Nowotny N, Zlinszky K, Ehrensperger F (2006) Shrews as reservoir hosts of borna disease virus. Emerg Infect Dis 12(4):675–677
Nobach D, Bourg M, Herzog S, Lange-Herbst H, Encarnacao JA, Eickmann M et al (2015) Shedding of infectious borna disease virus-1 in living bicolored white-toothed shrews. PLoS One 10(8):e0137018
Kinnunen PM, Inkeroinen H, Ilander M, Kallio ER, Heikkila HP, Koskela E et al (2011) Intracerebral Borna disease virus infection of bank voles leading to peripheral spread and reverse transcription of viral RNA. PLoS One 6(8):e23622
Biswal M, Ratho RK, Mishra B (2012) Role of reverse transcriptase polymerase chain reaction for the diagnosis of human rabies. Indian J Med Res 135(6):837–842
Sawtell NM, Thompson RL (2016) Herpes simplex virus and the lexicon of latency and reactivation: a call for defining terms and building an integrated collective framework. F1000Research 5:2038. doi:10.12688/f1000research.8886.1
Hoffmann B, Depner K, Schirrmeier H, Beer M (2006) A universal heterologous internal control system for duplex real-time RT-PCR assays used in a detection system for pestiviruses. J Virol Methods 136(1–2):200–209
Toussaint JF, Sailleau C, Breard E, Zientara S, De Clercq K (2007) Bluetongue virus detection by two real-time RT-qPCRs targeting two different genomic segments. J Virol Methods 140(1–2):115–123
Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74(12):5463–5467
Katoh K, Misawa K, Kuma K-I, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30:3059–3066
Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52(5):696–704
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S et al (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28(12):1647–1649
Acknowledgements
We thank Christian Korthase, Karin Pinger, Mareen Lange, Anke Mandelkow and Dörte Kaufmann at the Friedrich-Loeffler-Institut for excellent technical assistance. Furthermore, we are grateful to Sabine Ottinger-Kremer (Neustadt), Sabine Gallenberger (München), Jessica Hoch (Waiblingen), Anetta Hübsch (Heidelberg), Carina Spahr (Stuttgart), Hermann Ansorge (Görlitz), Stefan Bosch (Sternenfels), Anna Materna (Bad Nauheim), Christian Lynen (Oberhausen), Tanja Schäfer (Rödermark), Sonja Jonas (Billigheim), Jaqueline Gräfe (Dresden), Kerstin Janke (Wentorf), Katharina Volk (Leutenbach), M. Chevalier (Bonn), Tanya Lenn (Teltow) and Korinna Seybold (Bad König) for providing samples.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Funding information
This study has been supported in part by the EU Horizon 2020 program (European Commission Grant Agreement No. 643476 “COMPARE”).
Conflict of interest
The authors declare that there is no conflict of interest.
Ethical statements
None. All samples were collected as routine diagnostic measures.
Additional information
GenBank Accession Numbers: KY488722-KY488729 and KY508798-KY508804.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Schlottau, K., Hoffmann, B., Homeier-Bachmann, T. et al. Multiple detection of zoonotic variegated squirrel bornavirus 1 RNA in different squirrel species suggests a possible unknown origin for the virus. Arch Virol 162, 2747–2754 (2017). https://doi.org/10.1007/s00705-017-3432-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00705-017-3432-z