Evervac: phase I/II study of immunogenicity and safety of a new adjuvant-free TBE vaccine cultivated in Vero cell culture

References

• Demina TV, Dzhioev YP, Verkhozina MM, Kozlova IV, Tkachev SE, Plyusnin A, Doroshchenko EK, Lisak OV, Zlobin VI. Genotyping and characterization of the geographical distribution of tick-borne encephalitis virus variants with a set of molecular probes. J Med Virol. 2010;82(6):965–76. doi:10.1002/jmv.21765. PMID: 20419810.
   PubMed Web of Science ®Google Scholar
• Ruzek D, Avšič Županc T, Borde J, Chrdle A, Eyer L, Karganova G, Kholodilov I, Knap N, Kozlovskaya L, Matveev A, et al. Tick-borne encephalitis in Europe and Russia: review of pathogenesis, clinical features, therapy, and vaccines. Antiviral Res. 2019;164:23–51. doi:10.1016/j.antiviral.2019.01.014. PMID: 30710567.
   PubMed Web of Science ®Google Scholar
• Vorovitch MF, Maikova GB, Chernokhaeva LL, Romanenko VV, Karganova GG, Ishmukhametov AA. Comparison of the immunogenicity and safety of two pediatric TBE vaccines based on the Far Eastern and European virus subtypes. Adv Virol. 2019;24:5323428. doi:10.1155/2019/5323428. PMID: 31933642.
   Google Scholar
• Domnich A, Panatto D, Arbuzova EK, Signori A, Avio U, Gasparini R, Amicizia D. Immunogenicity against Far Eastern and Siberian subtypes of tick-borne encephalitis (TBE) virus elicited by the currently available vaccines based on European subtype: systematic review and meta-analysis. Hum Vaccine Immunoter. 2014;10(10):2818–33. doi:10.4161/hv.29984. PMID: 25483679.
   Web of Science ®Google Scholar
• Morozova OV, Bakhvalova VN, Potapova OF, Grishechkin AE, Isaeva EI, Aldarov KV, Klinov DV, Vorovich MF. Evaluation of immune response and protective effect of four vaccines against the tick-borne encephalitis virus. Vaccine. 2014;32(25):3101–06. doi:10.1016/j.vaccine.2014.02.046.
   PubMed Web of Science ®Google Scholar
• Chernokhaeva LL, Rogova YV, Kozlovskaya LI, Romanova LI, Osolodkin DI, Vorovitch MF, Karganova GG. Experimental evaluation of the protective efficacy of tick-borne encephalitis (TBE) vaccines based on European and Far-Eastern TBEV strains in mice and in vitro. Front Microbiol. 2018 16;9:1487. doi:10.3389/fmicb.2018.01487. PMID: 30061869.
   PubMed Web of Science ®Google Scholar
• Kollaritsch H, Paulke‐Korinek M, Holzmann H, Hombach J, Bjorvatn B, Barrett A. Vaccines and vaccination against tick‐borne encephalitis. Expert Rev Vaccines. 2012;11(9):1103‐1119. doi:10.1586/erv.12.86. PMID: 23151167.
   PubMed Web of Science ®Google Scholar
• Xing Y, Schmitt H-J, Arguedas A, Yang J. Tick-borne encephalitis in China: a review of epidemiology and vaccines. Vaccine. 2017;35(9):1227–37. doi:10.1016/j.vaccine.2017.01.015. PMID: 28153343.
   PubMed Web of Science ®Google Scholar
• WHO Expert Committee on biological standardization. Requirements for the use of animal cells as in vitro substrates for the production of biologicals. Geneva; 1998. WHO Technical Report No 878, annex 1. PMID: 9731464.
   Google Scholar
• WHO Expert Committee on biological standardization. Recommendations for the evaluation of animal cell cultures as substrates for the manufacture of biological medicinal products and for the characterization of cell banks. Geneva; 2010. WHO Technical Report Series 978, Annex 3.
   Google Scholar
• Genzel Y, Reichl U. Continuous cell lines as a production system for influenza vaccines. Expert Rev Vaccines. 2009;8(12):1681–92. doi:10.1586/erv.09.128. PMID: 19943763.
   PubMed Web of Science ®Google Scholar
• Tapia F, Vázquez-Ramírez D, Genzel Y, Reichl U. Bioreactors for high cell density and continuous multi-stage cultivations: options for process intensification in cell culture-based viral vaccine production. Appl Microbiol Biotechnol. 2016;100(5):2121–32. doi:10.1007/s00253-015-7267-9. PMID: 26758296.
   PubMed Web of Science ®Google Scholar
• Barrett P, Mundt W, Kistner O, Howard M. Vero cell platform in vaccine production: moving towards cell culture-based viral vaccines. Expert Rev Vaccines. 2009;8(5):607–18. doi:10.1586/erv.09.19. PMID: 19397417.
   PubMed Web of Science ®Google Scholar
• Toovey S. Preventing rabies with the Verorab® vaccine: 1985–2005 twenty years of clinical experience. Travel Med Infect Dis. 2007;5(6):327–48. doi:10.1016/j.tmaid.2007.07.004. PMID: 17983973.
   PubMedGoogle Scholar
• Ehrlich HJ, Müller M, Oh HML, Tambyah PA, Joukhadar C, Montomoli E, Fisher D, Berezuk G, Fritsch S, Löw-Baselli A, et al. A clinical trial of a whole-virus H5N1 vaccine derived from cell culture. N Engl J Med. 2008;358:2573–84. doi:10.1056/NEJMoa073121.
   PubMed Web of Science ®Google Scholar
• Kumar M, Sudeep AB, Arankalle VA. Evaluation of recombinant E2 protein-based and whole-virus inactivated candidate vaccines against chikungunya virus. Vaccine. 2012;30(43):6142–49. doi:10.1016/j.vaccine.2012.07.072. PMID: 22884660.
   PubMed Web of Science ®Google Scholar
• Monath TP, Liu J, Kanesa-thasan N, Myers GA, Nichols R, Deary A, McCarthy K, Johnson C, Ermak T, Shin S, et al. A live, attenuated recombinant West Nile virus vaccine. Proc Natl Acad Sci USA. 2006;103:6694–99. doi:10.1073/pnas.0601932103. PMID: 16617103.
   PubMed Web of Science ®Google Scholar
• Tauber E, Kollaritsch H, von Sonnenburg F, Lademann M, Jilma B, Firbas C, Jelinek T, Beckett C, Knobloch J, McBride W, et al. Randomized, double-blind, placebo-controlled Phase 3 trial of the safety and tolerability of IC51, an inactivated Japanese encephalitis vaccine. J Infect Dis. 2008;198:493–99. doi:10.1086/590116. PMID: 185888481.
   PubMed Web of Science ®Google Scholar
• Elbert BL, Terletskaya EN, Timofeev AV, Mironova LL, Khapchaev U, Amosenko FA, Svitkin YV, Alpatova GA, Krutyanskaya GL. Inactivated vaccine against tick-borne encephalitis (TBE) derived from heteroploid continuous monkey cell line. Vaccine. 1989;7(5):477. doi:10.1016/0264-410x(89)90183-7. PMID: 2815981.
   PubMed Web of Science ®Google Scholar
• Elbert BL, Vorovich MF, Terletskaya EN, Lisitsina EA, Atanadze SN, Sidorovich IG, Khozinskii VV, Tugizov S, Kushch AA, Khapchaev I, et al. Study of protective activity of preparations of TBE virus grown in different cell cultures. Zh Mikrobiol Epidemiol Immunobiol. 1992;1:25–28. PMID: 1414102. (in Russian).
   Google Scholar
• Khapchaev Y, Khoretonenko MV, Timofeev AV, Grachev VP. Reproduction of TBE virus Sofjin strain in Vero cells cultured on microcarriers under conditions of pseudo-suspension. Biotechnology. 2003;5:32–39. (in Russian).
   Google Scholar
• Vorovich MF, Khapchaev Y, Prilukova NS, Nagireva LI, Grachev VP. Russian inactivated liophilised TBE vaccine. Biopreparations Prev Diagnosis Treat. 2004;2:17–20. (in Russian).
   Google Scholar
• Vorovich MF, Kiktenko AV, Khapchaev Y, Grachev VP. The new inactivated vaccines against TBE virus. Zhurnal Infektsionnoy Patologii. 2012;19(3):13. (in Russian).
   Google Scholar
• Vorovitch MF, Kozlovskaya LI, Romanova L, Chernokhaeva LL, Ishmukhametov AA, Karganova GG. Genetic description of a tick-borne encephalitis virus strain Sofjin with the longest history as a vaccine strain. Springerplus. 2015;4:761. doi:10.1186/s40064-015-1561-y. PMID: 26682114.
   PubMedGoogle Scholar
• State register medicines. accessed 2020 Jan 28. https://grls.rosminzdrav.ru/CiPermitionReg.aspx?PermYear=0&DateInc=&NumInc=&DateBeg=&DateEnd=&Protocol=%d0%9a%d0%ad-%d0%92%d0%90%d0%9a-I%2fII-002%2f15+&RegNm=&Statement=&ProtoNum=&idCIStatementCh=&Qualifier=&CiPhase=&RangeOfApp=&Torg=&LFDos=&Producer=&Recearcher=&sponsorCountry=&MedBaseCount=&CiType=&PatientCount=&OrgDocOut=2&Status=&NotInReg=0&All=0&PageSize=8&order=date_perm&orderType=desc&pagenum=1.
   Google Scholar
• Khapchaev YK, Ivanova OE, Vorovitch MF, Romanenko VV, Makarov AE, Drozdov SG, Ishmukhametov AA. Comparative randomized study of tolerability, reactogenicity, immunogenicity and safety of the vaccine “BiVac Polio” (Oral Poliovirus vaccine type 1, 3). Epidemiol Vaccinal Prev. 2017;16(3):58–64. doi:10.31631/2073-3046-2017-16-3-58-64. (in Russian).
   Google Scholar
• Chernokhaeva LL, Maikova GB, Rogova Y, Romanenko VV, Ankudinova AV, Kilyachina AS, Vorovich MF, Karganova GG. Comparison of results obtained in ELISA and neutralization test in assessment of the protection of population from tick-borne encephalitis. Vopr Virusol. 2018;63(1):36–40. doi:10.18821/0507-4088-2018-63-1-36-40. (in Russian).
   PubMedGoogle Scholar
• Vorovitch MF, Maikova GB, Chernokhaeva LL, Romanenko VV, Ankudinova AV, Khapchaev Y, Karganova GG, Ishmukhametov AA, Drozdov SG. Immunogenicity and safety of the adult TBE vaccine “Tick-E-Vac”. Vopr Virusol. 2017;62(2):73–80. doi:10.18821/0507-4088-2017-62-2-73-80.
   PubMedGoogle Scholar
• Pereira RC, Silva AN, Souza MC, Silva МV, Neves PP, Silva AA, Matos DD, Herrera MA, Yamamura AM, Freire MS, et al. An inactivated yellow fever 17DD vaccine cultivated in Vero cell cultures. Vaccine. 2015;33(35):4261–68. doi:10.1016/j.vaccine.2015.03.077. PMID: 25862300.
   PubMed Web of Science ®Google Scholar
• Woods CW, Sanchez AM, Swamyc GK, McClain MT, Harrington L, Freeman D, Poore EA, Slifka DK, Poer DD, Amanna IJ, et al. An observer blinded, randomized, placebo-controlled, phase I dose escalation trial to evaluate the safety and immunogenicity of an inactivated West Nile virus Vaccine, HydroVax-001, in healthy adults. Vaccine. 2019;37:4222–30. doi:10.1016/j.vaccine.2018.12.026. PMID: 30661836.
   PubMed Web of Science ®Google Scholar
• Chernokhaeva LL, Rogova YV, Vorovitch MF, Romanova L, Kozlovskaya LI, Maikova GB, Kholodilov IS, Karganova GG. Protective immunity spectrum induced by immunization with a vaccine from the TBEV strain Sofjin. Vaccine. 2016;34(20):2354–61. doi:10.1016/j.vaccine.2016.03.041.
   PubMed Web of Science ®Google Scholar
• Pollabauer EM, Pavlova BG, Low-Baselli A, Fritsch S, Prymula R, Angermayr R, Draxler W, Firth C, Bosman J, Valenta B, et al. Comparison of immunogenicity and safety between two pediatric TBE vaccines. Vaccine. 2010;28:4680–85. doi:10.1016/j.vaccine.2010.04.047. PMID: 20433803.
   PubMed Web of Science ®Google Scholar
• Ankudinova AV, Romanenko VV, Vorovich MF, Kovtun OP, Esyunina MS, Kiktenko AV, Kilychina AS, Averyanov O. Results of a clinical immunogenicity and safety trial of Tick – E - Vac 0.25 ml vaccine (pediatric dosage). Vestnik Uralskoi Meditsinskoi Akademicheskoi Nauki. 2014;5(51):49–55. (in Russian).
   Google Scholar
• Feldblium V, Okuneva IA, Danilina TV, Menshikova MG, Pavroz KA, Trofimov DM, Ershov AE. Assessment of reactogenicity, safety and immunogenicity of the domestic vaccine ‘EnceVir’ with the reduced antigenic load in the immunization of children aged 3–17 years accordingly to routine scheduled vaccination (report 2). Epidemiol Infect Dis. 2015;20(3):28–32. (in Russian).
   Google Scholar
• Paulke-Korinek M, Kundi M, Laaber B, Brodtraeger N, Seidl-Friedrich C, Wiedermann U, Kollaritsch H. Factors associated with seroimmunity against tick borne encephalitis virus 10 years after booster vaccination. Vaccine. 2013;31(9):1293–97. doi:10.1016/j.vaccine.2012.12.075. PMID: 23306371.
   PubMed Web of Science ®Google Scholar
• Onishchenko GG, Krivulya SD, Fedorov Y, Pakskina ND, Skudareva ON, Kotova EA, Chernyavskaya OP, Ivanova AA, Arumova EA, Zhukov VI, et al. Sanitary and epidemiological rules SP 3.1.3.2352-08 Tick-borne viral encephalitis prevention. Bulletin of normative acts of federal executive bodies. Moscow: Rospotrebnadzor; 2008. p. 36 .
   Google Scholar
• Shoutova NA, Shkouratova OV, Rouzavina Y, Vlasova NM, Stavitskaya N, Vorobyova MS, Ladyzhenskaya IP, Solyanik RG. Studying immunologic activity and reactogenicity “EnceVir” vaccine immunization using express-scheme. Sibirskii Meditsinskii Zhurnal. 2009;24(2–2):30–33. (in Russian).
   Google Scholar
• Maikova GB, Chernokhaeva LL, Rogova YV, Kozlovskaya LI, Kholodilov IS, Vorovitch MF, Karganova GG, Romanenko VV, Esyunina MS, Ankudinova AA, et al. Ability of inactivated vaccines based on far-eastern tick-borne encephalitis virus strains to induce humoral immune response in originally seropositive and seronegative recipients. J Med Virol. 2019;91(2):190–200. doi:10.1002/jmv.25316. PMID: 30204244.
   PubMed Web of Science ®Google Scholar
• Zlatkovic J, Tsouchnikas G, Jarmer J, Koessl C, Stiasny K, Heinz FX. Aluminum hydroxide influences not only the extent but also the fine specificity and functional activity of antibody responses to tick-borne encephalitis virus in mice. J Virol. 2013;87(22):12187–95. doi:10.1128/JVI.01690-13. PMID: 24006434.
   PubMed Web of Science ®Google Scholar
• Haag CK, Dacey E, Hamilton N, White KP. Aluminum granuloma in a child secondary to DTaP-IPV vaccination: A case report. Pediatr Dermatol. 2019;36(1):e17–e19. doi:10.1111/pde.13732. Epub 2018 Nov 28. PMID: 30488642.
   PubMed Web of Science ®Google Scholar
• Bergfors E, Trollfors B. Sixty-four children with persistent itching nodules and contact allergy to aluminium after vaccination with aluminium-adsorbed vaccines – prognosis and outcome after booster vaccination. Eur J Pediatr. 2013;172(2):171–77. doi:10.1007/s00431-012-1841-2. Epub 2012 Oct 11. PMID: 23052615.
   PubMed Web of Science ®Google Scholar
• Masson JD, Crépeaux G, Authier FJ, Exley C, Gherardi RK. Critical analysis of reference studies on the toxicokinetics of aluminum-based adjuvants. J Inorg Biochem. 2018;181:87–95. doi:10.1016/j.jinorgbio.2017.12.015. Epub 2017 Dec 28. Review. PMID: 29307441.
   PubMed Web of Science ®Google Scholar