New World camelids are sentinels for the presence of Borna disease virus.
Borna disease virus
Bornavirus
New World camelids
alpaca
encephalitis
llama
Journal
Transboundary and emerging diseases
ISSN: 1865-1682
Titre abrégé: Transbound Emerg Dis
Pays: Germany
ID NLM: 101319538
Informations de publication
Date de publication:
Mar 2022
Mar 2022
Historique:
revised:
15
01
2021
received:
06
08
2020
accepted:
22
01
2021
pubmed:
28
1
2021
medline:
1
4
2022
entrez:
27
1
2021
Statut:
ppublish
Résumé
Borna disease (BD), a frequently fatal neurologic disorder caused by Borna disease virus 1 (BoDV-1), has been observed for decades in horses, sheep, and other mammals in certain regions of Europe. The bicoloured white-toothed shrew (Crocidura leucodon) was identified as a persistently infected species involved in virus transmission. Recently, BoDV-1 attracted attention as a cause of fatal encephalitis in humans. Here, we report investigations on BoDV-1-infected llamas from a farm in a BD endemic area of Switzerland, and alpacas from holdings in a region of Germany where BD was last seen in the 1960s but not thereafter. All New World camelids showed apathy and abnormal behaviour, necessitating euthanasia. Histologically, severe non-suppurative meningoencephalitis with neuronal Joest-Degen inclusion bodies was observed. BoDV-1 was confirmed by immunohistology, RT-qPCR, and sequencing in selected animals. Analysis of the llama herd over 20 years showed that losses due to clinically suspected BD increased within the last decade. BoDV-1 whole-genome sequences from one Swiss llama and one German alpaca and-for comparison-from one Swiss horse and one German shrew were established. They represent the first published whole-genome sequences of BoDV-1 clusters 1B and 3, respectively. Our analysis suggests that New World camelids may have a role as a sentinel species for BoDV-1 infection, even when symptomatic cases are lacking in other animal species.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
451-464Informations de copyright
© 2021 The Authors. Transboundary and Emerging Diseases published by Wiley-VCH GmbH.
Références
Altmann, D., Kronberger, H., Schüppel, K., Lippmann, R., & Altmann, I. (1976). Bornasche Krankheit (Meningo-encephalomyelitis simplex enzootica equorum) bei Neuwelttylopoden und Equiden. Vol. 18, p. 132. In: Verhandlungsberichte des 18. Int. Symp. über Erkrankungen der Zoo- und Wildtiere. (in German)
Briese, T., de la Torre, J. C., Lewis, A., Ludwig, H., & Lipkin, W. I. (1992). Borna disease virus, a negative-strand RNA virus, transcribes in the nucleus of infected cells. Proceedings National Academy Sciences of the United States of America, 89, 11486-11489.
Briese, T., Schneemann, A., Lewis, A. J., Park, Y. S., Kim, S., Ludwig, H., & Lipkin, W. I. (1994). Genomic organization of Borna disease virus. Proceedings National Academy Sciences of the United States of America, 91, 4362-4366. https://doi.org/10.1073/pnas.91.10.4362
Caplazi, P., & Ehrensperger, F. (1998). Spontaneous Borna disease in sheep and horses: Immunophenotyping of inflammatory cells and detection of MHC-I and MHC-II antigen expression in Borna encephalitis lesions. Veterinary Immunology and Immunopathology, 61, 203-220. https://doi.org/10.1016/S0165-2427(97)00128-1
Caplazi, P., Melzer, K., Goetzmann, R., Rohner-Cotti, A., Bracher, V., Zlinszky, K., & Ehrensperger, F. (1999). Die “Bornasche Krankheit” in der Schweiz und im Fürstentum Liechtenstein [Borna disease in Switzerland and in the principality of Liechtenstein]. Schweizer Archiv Fur Tierheilkunde, 141, 521-527.(in German)
Coras, R., Korn, K., Kuerten, S., Huttner, H. B., & Ensser, A. (2019). Severe bornavirus-encephalitis presenting as Guillain-Barré-syndrome. Acta Neuropathologica, 137, 1017-1019. https://doi.org/10.1007/s00401-019-02005-z
Dürrwald, R. (1993). 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. Dissertation, Freie Universität Berlin, Germany (in German).
Dürrwald, R., Kolodziejek, J., Muluneh, A., Herzog, S., & Nowotny, N. (2006). 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 and Infection, 8, 917-929. https://doi.org/10.1016/j.micinf.2005.08.013
Dürrwald, R., Kolodziejek, J., Weissenböck, H., & Nowotny, N. (2014). The bicolored white-toothed shrew Crocidura leucodon is an indigenous host of mammalian Borna disease virus. PLoS One, 9, e93659. https://doi.org/10.1371/journal.pone.0093659
Dürrwald, R., & Ludwig, H. (1997). 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, 44, 147-184.
Herzog, S., Enderlein, D., Heffels-Redmann, U., Piepenbring, A., Neumann, D., Kaleta, E. F., Muller, H., Lierz, M., & Herden, C. (2010). Indirect immunofluorescence assay for intra vitam diagnosis of avian bornavirus infection in psittacine birds. Journal of Clinical Microbiology, 48, 2282-2284. https://doi.org/10.1128/jcm.00145-10
Hilbe, M., Herrsche, R., Kolodziejek, J., Nowotny, N., Zlinszky, K., & Ehrensperger, F. (2006). Shrews as reservoir hosts of Borna disease virus. Emerging Infectious Diseases, 12, 675-677. https://doi.org/10.3201/eid1204.051418
Hoffmann, B., Tappe, D., Höper, D., Herden, C., Boldt, A., Mawrin, C., Niederstraßer, O., Müller, T., Jenckel, M., van der Grinten, E., Lutter, C., Abendroth, B., Teifke, J. P., Cadar, D., Schmidt-Chanasit, J., Ulrich, R. G., & Beer, M. (2015). A variegated squirrel Bornavirus associated with fatal human encephalitis. New England Journal of Medicine, 373, 154-162. https://doi.org/10.1056/NEJMoa1415627
Honkavuori, K. S., Shivaprasad, H. L., Williams, B. L., Quan, P.-L., Hornig, M., Street, C., Palacios, G., Hutchison, S. K., Franca, M., Egholm, M., Briese, T., & Lipkin, W. I. (2008). Novel Borna virus in psittacine birds with proventricular dilatation disease. Emerging Infectious Diseases, 14, 1883-1886. https://doi.org/10.3201/eid1412.080984
Horie, M., Honda, T., Suzuki, Y., Kobayashi, Y., & Tomonaga, K. (2010). Endogenous non-retroviral RNA virus elements in mammalian genomes. Nature, 463, 84-87. https://doi.org/10.1038/nature08695.Endogenous
Hyndman, T. H., Shilton, C. M., Stenglein, M. D., & Wellehan, J. F. X. (2018). Divergent bornaviruses from Australian carpet pythons with neurological disease date the origin of extant Bornaviridae prior to the end-Cretaceous extinction. PLoS Path, 14, e1006881. https://doi.org/10.1371/journal.ppat.1006881
Ihlenburg, H., & Brehmer, H. (1964). Beitrag zur latenten Borna-Erkrankung des Pferdes. Monatsh Veterinaermed, 19, 463-465.(in German)
Jacobsen, B., Algermissen, D., Schaudien, D., Venner, M., Herzog, S., Wentz, E., Hewicker-Trautwein, M., Baumgärtner, W., & Herden, C. (2010). Borna disease in an adult alpaca stallion (Lama pacos). Journal of Comparative Pathology, 143, 203-208. https://doi.org/10.1016/j.jcpa.2010.01.009
Joest, E., & Degen, K. (1909). Über eigentümliche Kerneinschlüsse der Ganglienzellen bei der enzootischen Gehirn-Rückenmarksentzündung der Pferde. Zeitschrift Infekt. Der Haustiere, 6, 348-356.(in German)
Kistler, A. L., Gancz, A., Clubb, S., Skewes-Cox, P., Fischer, K., Sorber, K., Chiu, C. Y., Lublin, A., Mechani, S., Farnoushi, Y., Greninger, A., Wen, C. C., Karlene, S. B., Ganem, D., & DeRisi, J. L. (2008). Recovery of divergent avian bornaviruses from cases of proventricular dilatation disease: Identification of a candidate etiologic agent. Virology Journal, 5, 1-15. https://doi.org/10.1186/1743-422X-5-88
Kobera, R. (2016). Bornaerkrankung und Kuhpocken bei Alpakas. pp. 18-19.In: Int. New World Camelid Meet.
Kobera, R., & Poehle, D. (2004). Case reports in South American camelids in Germany. p. 151. In: Proc. 4th Eur. Symp. South Am. Camelids DECAMA Eur. Semin.
Kolodziejek, J., Dürrwald, R., Herzog, S., Ehrensperger, F., Lussy, H., & Nowotny, N. (2005). Genetic clustering of Borna disease virus natural animal isolates, laboratory and vaccine strains strongly reflects their regional geographical origin. Journal of General Virology, 86, 385-398. https://doi.org/10.1099/vir.0.80587-0
Korn, K., Coras, R., Bobinger, T., Herzog, S. M., Lücking, H., Stöhr, R., Huttner, H. B., Hartmann, A., & Ensser, A. (2018). Fatal encephalitis associated with Borna disease virus 1. New England Journal of Medicine, 379, https://doi.org/10.1056/NEJMc1500960
Kuhn, J. H., Dürrwald, R., Bào, Y., Briese, T., Carbone, K., Clawson, A. N., deRisi, J. L., Garten, W., Jahrling, P. B., Kolodziejek, J., Rubbenstroth, D., Schwemmle, M., Stenglein, M., Tomonaga, K., Weissenböck, H., & Nowotny, N. (2015). Taxonomic reorganization of the family Bornaviridae. Archives of Virology, 160, 621-632. https://doi.org/10.1007/s00705-014-2276-z
Kumar, S., Stecher, G., Li, M., Knyaz, C., & Tamura, K. (2018). MEGA X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35, 1547-1549. https://doi.org/10.1093/molbev/msy096
Liesche, F., Ruf, V., Zoubaa, S., Kaletka, G., Rosati, M., Rubbenstroth, D., Herden, C., Goehring, L., Wunderlich, S., Wachter, M. F., Rieder, G., Lichtmannegger, I., Permanetter, W., Heckmann, J. G., Angstwurm, K., Neumann, B., Märkl, B., Haschka, S., Niller, H. H., … Schlegel, J. (2019). The neuropathology of fatal encephalomyelitis in human Borna virus infection. Acta Neuropathologica, 138, 653-665. https://doi.org/10.1007/s00401-019-02047-3
Niller, H. H., Angstwurm, K., Rubbenstroth, D., Schlottau, K., Ebinger, A., Giese, S., Wunderlich, S., Banas, B., Forth, L. F., Hoffmann, D., Höper, D., Schwemmle, M., Tappe, D., Schmidt-Chanasit, J., Nobach, D., Herden, C., Brochhausen, C., Velez-Char, N., Mamilos, A., … Schmidt, B. (2020). Zoonotic spillover infections with Borna disease virus 1 leading to fatal human encephalitis, 1999-2019: An epidemiological investigation. The Lancet Infectious Diseases, 3099, 9-14. https://doi.org/10.1016/s1473-3099(19)30546-8
Nobach, D., Bourg, M., Herzog, S., Lange-Herbst, H., Encarnação, J. A., Eickmann, M., & Herden, C. (2015). Shedding of infectious Borna disease virus-1 in living bicolored white-toothed shrews. PLoS One, 10, e0137018. https://doi.org/10.1371/journal.pone.0137018
Nowotny, N., Kolodziejek, J., Jehle, C. O., Suchy, A., Staeheli, P., & Schwemmle, M. (2002). Isolation and characterization of a new subtype of Borna disease virus. Journal of Virology, 74, 5655-5658. https://doi.org/10.1128/jvi.74.12.5655-5658.2000
Richt, J. A., Pfeuffer, I., Christ, M., Frese, K., Bechter, K., & Herzog, S. (1997). Borna disease virus infection in animals and humans. Emerging Infectious Diseases, 3, 343-352. https://doi.org/10.3201/eid0303.970311
Rubbenstroth, D., Schlottau, K., Schwemmle, M., Rissland, J., & Beer, M. (2019). Human bornavirus research: Back on track!. PLoS Path, 15, 1-5. https://doi.org/10.1371/journal.ppat.1007873
Schindler, A. R., Vögtlin, A., Hilbe, M., Puorger, M., Zlinszky, K., Ackermann, M., & Ehrensperger, F. (2007). Reverse transcription real-time PCR assays for detection and quantification of Borna disease virus in diseased hosts. Molecular and Cellular Probes, 21, 47-55. https://doi.org/10.1016/j.mcp.2006.08.001
Schlottau, K., Forth, L., & Beer, M. (2018). Fatal encephalitic Borna disease virus 1 in solid-organ transplant recipients. New England Journal of Medicine, 379, 1377-1379. https://doi.org/10.1056/NEJMc1800724
Schmidt, J. (1912). Untersuchungen über das klinische Verhalten der seuchenhaften Gehirnrückenmarksentzündung (Bornaschen Krankheit) des Pferdes nebst Angaben über diesbezügliche therapeutische Versuche [Investigation into the clinical behaviour of epidemic encephalomyelitis. Berl Tieraerztl Wochenscrift, 28, 581-586.(in German)
Schulze, V., Große, R., Fürstenau, J., Forth, L. F., Ebinger, A., Richter, M. T., Tappe, D., Mertsch, T., Klose, K., Schlottau, K., Hoffmann, B., Höper, D., Mundhenk, L., Ulrich, R. G., Beer, M., Müller, K.-E., & Rubbenstroth, D. (2020). Borna disease outbreak with high mortality in an alpaca herd in a previously unreported endemic area in Germany. Transboundary and Emerging Diseases, 2093-2107. https://doi.org/10.1111/tbed.13556
Schüppel, K., Kinne, J., & Reinacher, M. (1994). Bornavirus-Antigennachweis bei Alpakas (Lama pakos) sowie bei einem Faultier (Choloepus didactylus) und einem Zwergflussferd (Choeropsis liberiensis). pp. 189-194.In: Verhbericht XXXVI Int Symp Erkrankg Zootiere. (in German)
Shi, M., Lin, X. D., Chen, X., Tian, J. H., Chen, L. J., Li, K., Wang, W., Eden, J. S., Shen, J. J., Liu, L., Holmes, E. C., & Zhang, Y. Z. (2018). The evolutionary history of vertebrate RNA viruses. Nature, 556, 197-202. https://doi.org/10.1038/s41586-018-0012-7
Stenglein, M. D., Leavitt, E. B., Abramovitch, M. A., McGuire, J. A., & DeRisi, J. L. (2014). Genome sequence of a bornavirus recovered from an African Garter Snake (Elapsoidea loveridgei). Genome Announc., 2, https://doi.org/10.1128/genomeA.00779-14
Tizard, I., Ball, J., Stoica, G., & Payne, S. (2016). The pathogenesis of bornaviral diseases in mammals. Animal Health Research Reviews, 17, 92-109. https://doi.org/10.1017/S1466252316000062
Weissenböck, H., Bagó, Z., Kolodziejek, J., Hager, B., Palmetzhofer, G., Dürrwald, R., & Nowotny, N. (2017). Infections of horses and shrews with Bornaviruses in Upper Austria: A novel endemic area of Borna disease. Emerging Microbes & Infections, 6, e52. https://doi.org/10.1038/emi.2017.36
Weissenböck, H., Bakonyi, T., Sekulin, K., Ehrensperger, F., Doneley, R. J., Dürrwald, R., Hoop, R., Erdélyi, K., Gál, J., Kolodziejek, J., & Nowotny, N. (2009). Avian bornaviruses in psittacine birds from Europe and Australia with proventricular dilatation disease. Emerging Infectious Diseases, 15, 1453-1459. https://doi.org/10.3201/eid1509.090353
Whitehead, C. E., & Bedenice, D. (2009). Neurologic diseases in llamas and alpacas. Veterinary Clinics of North America: Food Animal Practice, 25, 385-405. https://doi.org/10.1016/j.cvfa.2009.02.004