{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,19]],"date-time":"2026-10-19T16:44:15Z","timestamp":1792428255332,"version":"4.5.0"},"reference-count":42,"publisher":"MDPI AG","issue":"10","license":[{"start":{"date-parts":[[2019,10,11]],"date-time":"2019-10-11T00:00:00Z","timestamp":1570752000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Viruses"],"abstract":"<jats:p>Human rabies vaccines have been shown to induce partial protection against members of phylogroup I bat lyssaviruses. Here, we investigated the capacity of a widely used rabies inactivated vaccine (Rabisin, Boehringer-Ingelheim) for veterinary use to cross-protect mice experimentally infected with European bat lyssavirus 1 (EBLV-1b), European bat lyssavirus 2 (EBLV-2), and Bokeloh bat lyssavirus (BBLV) occurring in Europe. For each lyssavirus, we investigated the efficacy of two different doses of vaccine against two viral doses administrated by either central or peripheral routes. In parallel, seroconversion following pre-exposure vaccination was investigated. In this study, we demonstrated that the three investigated bat isolates were pathogenic, even at low dose, when inoculated by the central route but were not\/less pathogenic when administrated peripherally. The Rabisin vaccine was capable of significantly cross-protecting mice inoculated intramuscularly with EBLV-1b and EBLV-2 and intracerebrally with BBLV. The level of rabies neutralizing antibodies induced by the Rabisin was quite high against the bat lyssaviruses, but with no significant differences between immunization with 1 and 5 IU\/dose. The study emphasizes that the quality of rabies-inactivated vaccines for veterinary use is of utmost importance to optimize the cross-protection of pets against phylogroup I bat lyssaviruses occurring in Europe.<\/jats:p>","DOI":"10.3390\/v11100936","type":"journal-article","created":{"date-parts":[[2019,10,11]],"date-time":"2019-10-11T10:53:03Z","timestamp":1570791183000},"page":"936","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":9,"title":["Cross-Protection of Inactivated Rabies Vaccines for Veterinary Use against Bat Lyssaviruses Occurring in Europe"],"prefix":"10.3390","volume":"11","author":[{"given":"Alexandre","family":"Servat","sequence":"first","affiliation":[{"name":"French Agency for Food, Environmental and Occupational Health & Safety (ANSES), Nancy Laboratory for Rabies and Wildlife, OIE Reference Laboratory for Rabies, European Union Reference Laboratory for Rabies, European Union Reference Laboratory for Rabies Serology, Technop\u00f4le Agricole et V\u00e9t\u00e9rinaire, Domaine de Pix\u00e9r\u00e9court, CS 40009, 54220 Malz\u00e9ville, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marine","family":"Wasniewski","sequence":"additional","affiliation":[{"name":"French Agency for Food, Environmental and Occupational Health & Safety (ANSES), Nancy Laboratory for Rabies and Wildlife, OIE Reference Laboratory for Rabies, European Union Reference Laboratory for Rabies, European Union Reference Laboratory for Rabies Serology, Technop\u00f4le Agricole et V\u00e9t\u00e9rinaire, Domaine de Pix\u00e9r\u00e9court, CS 40009, 54220 Malz\u00e9ville, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Florence","family":"Cliquet","sequence":"additional","affiliation":[{"name":"French Agency for Food, Environmental and Occupational Health & Safety (ANSES), Nancy Laboratory for Rabies and Wildlife, OIE Reference Laboratory for Rabies, European Union Reference Laboratory for Rabies, European Union Reference Laboratory for Rabies Serology, Technop\u00f4le Agricole et V\u00e9t\u00e9rinaire, Domaine de Pix\u00e9r\u00e9court, CS 40009, 54220 Malz\u00e9ville, France"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2019,10,11]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1016\/j.tvjl.2014.10.026","article-title":"Terrestrial rabies control in the European Union: Historical achievements and challenges ahead","volume":"203","author":"Mueller","year":"2015","journal-title":"Vet. J."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"905","DOI":"10.1586\/14787210.2014.921570","article-title":"Rabies in Europe: What are the risks?","volume":"12","author":"Cliquet","year":"2014","journal-title":"Expert Rev. Anti-Infect. Ther."},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Shipley, R., Wright, E., Selden, D., Wu, G., Aegerter, J., Fooks, A.R., and Banyard, A.C. (2019). Bats and Viruses: Emergence of Novel Lyssaviruses and Association of Bats with Viral Zoonoses in the EU. Trop. Med. Infect. Dis., 4.","DOI":"10.3390\/tropicalmed4010031"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"2974","DOI":"10.3390\/v6082974","article-title":"Lyssaviruses and Bats: Emergence and Zoonotic Threat","volume":"6","author":"Banyard","year":"2014","journal-title":"Viruses"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1111\/zph.12003","article-title":"Molecular Epidemiology of Bat Lyssaviruses in Europe: Molecular Epidemiology of EBLV","volume":"60","author":"McElhinney","year":"2013","journal-title":"Zoonoses Public Health"},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Picard-Meyer, E., Robardet, E., Arthur, L., Larcher, G., Harbusch, C., Servat, A., and Cliquet, F. (2014). Bat Rabies in France: A 24-Year Retrospective Epidemiological Study. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0098622"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1263","DOI":"10.3201\/1408.080068","article-title":"Endemic Circulation of European Bat Lyssavirus Type 1 in Serotine Bats, Spain","volume":"14","author":"Juste","year":"2008","journal-title":"Emerg. Infect. Dis."},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Moldal, T., Vik\u00f8ren, T., Cliquet, F., Marston, D.A., van der Kooij, J., Madslien, K., and \u00d8rpetveit, I. (2017). First detection of European bat lyssavirus type 2 (EBLV-2) in Norway. BMC Vet. Res., 13.","DOI":"10.1186\/s12917-017-1135-z"},{"key":"ref_9","first-page":"1519","article-title":"Novel Lyssavirus in Natterer\u2019s Bat, Germany","volume":"17","author":"Freuling","year":"2011","journal-title":"Emerg. Infect. Dis."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"2333","DOI":"10.1007\/s00705-013-1747-y","article-title":"Isolation of Bokeloh bat lyssavirus in Myotis nattereri in France","volume":"158","author":"Servat","year":"2013","journal-title":"Arch. Virol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1015","DOI":"10.1111\/zph.12519","article-title":"Bokeloh bat lyssavirus isolation in a Natterer\u2019s bat, Poland","volume":"65","author":"Smreczak","year":"2018","journal-title":"Zoonoses Public Health"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"793","DOI":"10.3201\/eid1905.121071","article-title":"Novel Lyssavirus in Bat, Spain","volume":"19","author":"Ceballos","year":"2013","journal-title":"Emerg. Infect. Dis."},{"key":"ref_13","first-page":"254","article-title":"Lleida Bat Lyssavirus isolation in Miniopterus schreibersii in France","volume":"66","author":"Beven","year":"2018","journal-title":"Zoonoses Public Health"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"593","DOI":"10.1111\/tbed.12833","article-title":"Tentative novel lyssavirus in a bat in Finland","volume":"65","author":"Nokireki","year":"2018","journal-title":"Transbound. Emerg. Dis."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"280","DOI":"10.3201\/eid1502.080637","article-title":"European Bat Lyssavirus Transmission among Cats, Europe","volume":"15","author":"Dacheux","year":"2009","journal-title":"Emerg. Infect. Dis."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1111\/j.1439-0450.2003.00725.x","article-title":"Spill-over of European Bat Lyssavirus Type 1 into a Stone Marten (Martes foina) in Germany","volume":"51","author":"Cox","year":"2004","journal-title":"J. Vet. Med. Ser. B"},{"key":"ref_17","first-page":"15","article-title":"A new case of European Bat Lyssavirus (EBL) infection in Danish sheep","volume":"26","author":"Ronsholt","year":"2002","journal-title":"Rabies Bull. Eur."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1029","DOI":"10.1017\/S0950268803001481","article-title":"European bat lyssaviruses: An emerging zoonosis","volume":"131","author":"Fooks","year":"2003","journal-title":"Epidemiol. Infect."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1647","DOI":"10.1099\/vir.0.065953-0","article-title":"Comparative studies on the genetic, antigenic and pathogenic characteristics of Bokeloh bat lyssavirus","volume":"95","author":"Nolden","year":"2014","journal-title":"J. Gen. Virol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"4101","DOI":"10.1016\/j.vaccine.2005.03.037","article-title":"Rabies human diploid cell vaccine elicits cross-neutralising and cross-protecting immune responses against European and Australian bat lyssaviruses","volume":"23","author":"Brookes","year":"2005","journal-title":"Vaccine"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"64","DOI":"10.1186\/s13028-017-0332-x","article-title":"Efficacy of rabies vaccines in dogs and cats and protection in a mouse model against European bat lyssavirus type 2","volume":"59","author":"Nokireki","year":"2017","journal-title":"Acta Vet. Scand."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1016\/j.virusres.2005.03.009","article-title":"Efficacy of rabies biologics against new lyssaviruses from Eurasia","volume":"111","author":"Hanlon","year":"2005","journal-title":"Virus Res."},{"key":"ref_23","unstructured":"(2019, August 22). European Bat Lyssavirus 2 Isolate RV1332 Glycoprotein (G.) mRNA, Partial Cds, Available online: http:\/\/www.ncbi.nlm.nih.gov\/nuccore\/GU936871.1."},{"key":"ref_24","unstructured":"(2019, August 22). Bokeloh Bat Lyssavirus Isolate 129700, Complete Genome, Available online: http:\/\/www.ncbi.nlm.nih.gov\/nuccore\/KC169985.1."},{"key":"ref_25","unstructured":"Wilbur, L., and Aubert, M.F. (1996). Laboratory techniques in rabies: The NIH test for potency. Laboratory Techniques in Rabies, World Health Organization. [4th ed.]."},{"key":"ref_26","unstructured":"Council of Europe (2013). Rabies Vaccine (Inactivated) for Veterinary Use, Monograph 0451. European Pharmacopoeia, Council of Europe. [8th ed.]."},{"key":"ref_27","first-page":"57","article-title":"EDQM biological reference preparation for rabies vaccine (inactivated) for veterinary use","volume":"2015","author":"Daas","year":"2015","journal-title":"Pharmeuropa Bio. Sci. Notes"},{"key":"ref_28","unstructured":"European Commission (2010). Directive 2010\/63\/EU of the European Parliament and of the Council of 22 September 2010 on the Protection of Animals Used for Scientific Purposes, European Commission."},{"key":"ref_29","unstructured":"Officiel de la R\u00e9publique Fran\u00e7aise (2013). D\u00e9cret n 2013-118 Du 1er F\u00e9vrier 2013 Relatif \u00e0 La Protection des Animaux Utilis\u00e9s \u00e0 Des Fins Scientifiques, Journal Officiel de la R\u00e9publique Fran\u00e7aise."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"429","DOI":"10.1177\/026119290303100409","article-title":"Three Rs approaches in the quality control of inactivated rabies vaccines. The report and recommendations of ECVAM workshop 48","volume":"31","author":"Bruckner","year":"2003","journal-title":"Altern. Lab. Anim. ATLA"},{"key":"ref_31","unstructured":"Rupprecht, C.E., Fooks, A.R., and Abela-Ridder, B. (2019). The Direct Fluorescent Antibody Test. Laboratory Techniques in Rabies, World Health Organization."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1016\/j.jviromet.2014.04.005","article-title":"Use of filter paper blood samples for rabies antibody detection in foxes and raccoon dogs","volume":"204","author":"Wasniewski","year":"2014","journal-title":"J. Virol. Methods"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1016\/j.biologicals.2011.12.011","article-title":"Evaluation of a rapid immunochromatographic diagnostic test for the detection of rabies from brain material of European mammals","volume":"40","author":"Servat","year":"2012","journal-title":"Biologicals"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1016\/S0022-1759(97)00212-3","article-title":"Development of a fluorescent antibody virus neutralisation test (FAVN test) for the quantitation of rabies-neutralising antibody","volume":"212","author":"Cliquet","year":"1998","journal-title":"J. Immunol. Methods"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"779","DOI":"10.20506\/rst.36.3.2713","article-title":"Production and calibration of the second batch of OIE anti-rabies positive reference serum: -EN- -FR- Production et \u00e9talonnage du second lot de s\u00e9rum de r\u00e9f\u00e9rence positif de l\u2019OIE pour la rage -ES- Producci\u00f3n y calibraci\u00f3n del segundo lote de suero positivo antirr\u00e1bico de referencia de la OIE","volume":"36","author":"Wasniewski","year":"2017","journal-title":"Rev. Sci. Tech. OIE"},{"key":"ref_36","first-page":"839518","article-title":"Cross-Platform Evaluation of Commercial Real-Time SYBR Green RT-PCR Kits for Sensitive and Rapid Detection of European Bat Lyssavirus Type 1","volume":"2015","author":"Schereffer","year":"2015","journal-title":"BioMed Res. Int."},{"key":"ref_37","unstructured":"World Health Organization (2018). WHO Expert Consultation on Rabies: Third Report, World Health Organization."},{"key":"ref_38","unstructured":"World Health Organization (2005). WHO Expert Consultation on Rabies: First Report, World Health Organization."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"362","DOI":"10.1016\/0264-410X(88)90184-3","article-title":"Immunity against the European bat rabies (Duvenhage) virus induced by rabies vaccines: An experimental study in mice","volume":"6","author":"Lafon","year":"1988","journal-title":"Vaccine"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1177\/026119291504300106","article-title":"A step forward in the quality control testing of inactivated rabies vaccines\u2014Extensive evaluation of European vaccines by using alternative methods to the in vivo potency tests","volume":"43","author":"Servat","year":"2015","journal-title":"Altern. Lab. Anim. ATLA."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1278","DOI":"10.1002\/jps.21523","article-title":"Vaccine adjuvants: Current challenges and future approaches","volume":"98","author":"Torres","year":"2009","journal-title":"J. Pharm. Sci."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"2285","DOI":"10.1016\/j.vaccine.2019.03.037","article-title":"Avoiding preventable deaths: The scourge of counterfeit rabies vaccines","volume":"37","author":"Taylor","year":"2019","journal-title":"Vaccine"}],"container-title":["Viruses"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1999-4915\/11\/10\/936\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T13:25:26Z","timestamp":1760189126000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1999-4915\/11\/10\/936"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,10,11]]},"references-count":42,"journal-issue":{"issue":"10","published-online":{"date-parts":[[2019,10]]}},"alternative-id":["v11100936"],"URL":"https:\/\/doi.org\/10.3390\/v11100936","relation":{},"ISSN":["1999-4915"],"issn-type":[{"value":"1999-4915","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,10,11]]}}}