Immune response to live-attenuated Japanese encephalitis vaccine (JE-CV) neutralizes Japanese encephalitis virus isolates from south-east Asia and India

Matthew Bonaparte, Bashir Dweik, Emmanuel Feroldi, Claude Meric, Alain Bouckenooghe, Stephen Hildreth, Branda Hu, Sutee Yoksan, Mark Boaz, Matthew Bonaparte, Bashir Dweik, Emmanuel Feroldi, Claude Meric, Alain Bouckenooghe, Stephen Hildreth, Branda Hu, Sutee Yoksan, Mark Boaz

Abstract

Background: During clinical development of the licensed Japanese encephalitis chimeric virus vaccine (JE-CV), the neutralization capacity of vaccine-induced antibodies was assessed against the vaccine virus and against well characterized wild-type (wt) viruses isolated between 1949-1991. We assessed whether JE-CV-induced antibodies can also neutralize more recent wt Japanese encephalitis virus (JEV) isolates including a genotype 1 isolate.

Methods: Sera from 12-18 month-old children who received a single dose of JE-CV in a phase III study in Thailand and the Philippines (ClinicalTrials.gov NCT00735644) were randomly selected and pooled according to neutralization titer against JE-CV into eight samples. Neutralization was assessed by plaque reduction neutralization tests (PRNT50) against three recent isolates from JEV genotypes 1 and 3 in addition to four JEV previously tested.

Results: Neutralization titers against the three recent JEV strains were comparable to those observed previously against other strains and the vaccine virus. The observed differences between responses to genotype 1 and 3 viruses were within assay variability for the PRNT50.

Conclusions: The results were consistent with previously generated data on the neutralization of wt JEV isolates, immune responses induced by JE-CV neutralize recently isolated virus from southeast (SE) Asia and India.

Figures

Figure 1
Figure 1
Geometric mean titers for the sera pools against the different JEV.

References

    1. Halstead SB, Jacobson J. In: Vaccines. 5. Plotkin SA, Orenstein WA, Offit PA, editor. Philadelphia (PA): Saunders Elsevier; 2008. Japanese encephalitis vaccines; pp. 311–352.
    1. Mackenzie JS, Gubler DJ, Petersen LR. Emerging flaviviruses: the spread and resurgence of Japanese encephalitis, West Nile and dengue viruses. Nat Med. 2004;14(12 Suppl):S98–S109.
    1. Beasley DW, Lewthwaite P, Solomon T. Current use and development of vaccines for Japanese encephalitis. Expert Opin Biol Ther. 2008;14(1):95–106. doi: 10.1517/14712598.8.1.95.
    1. Halstead SB, Thomas SJ. New Japanese encephalitis vaccines: alternatives to production in mouse brain. Expert Rev Vaccines. 2011;14(3):355–364. doi: 10.1586/erv.11.7.
    1. Monath TP, Guirakhoo F, Nichols R, Yoksan S, Schrader R, Murphy C, Blum P, Woodward S, McCarthy K, Mathis D, Johnson C, Bedford P. Chimeric, live, attenuated vaccine against Japanese encephalitis (ChimeriVax-JE): phase 2 clinical trials for safety and immunogenicity, effect of vaccine dose and schedule, and memory response to challenge with inactivated Japanese encephalitis antigen. J Infect Dis. 2003;14(8):1213–1230. doi: 10.1086/378356.
    1. Monath TP, McCarthy K, Bedford P, Johnson CT, Nichols R, Yoksan S, Marchesani R, Knauber M, Wells KH, Arroyo J, Guirakhoo F. Clinical proof of principle for ChimeriVax: recombinant live, attenuated vaccines against flavivirus infections. Vaccine. 2002;14(7–8):1004–1018.
    1. Torresi J, McCarthy K, Feroldi E, Méric C. Immunogenicity, safety and tolerability in adults of a new single-dose, live-attenuated vaccine against Japanese encephalitis: Randomised controlled phase 3 trials. Vaccine. 2010;14(50):7993–8000. doi: 10.1016/j.vaccine.2010.09.035.
    1. Chokephaibulkit K, Sirivichayakul C, Thisyakorn U, Sabchareon A, Pancharoen C, Bouckenooghe A, Gailhardou S, Boaz M, Feroldi E. Safety and immunogenicity of a single administration of live-attenuated Japanese encephalitis vaccine in previously primed 2- to 5-year-olds and naive 12- to 24-month-olds: multicenter randomized controlled trial. Pediatr Infect Dis J. 2010;14(12):1111–1117. doi: 10.1097/INF.0b013e3181f68e9c.
    1. Chen WR, Tesh RB, Rico-Hesse R. Genetic variation of Japanese encephalitis virus in nature. J Gen Virol. 1990;14:2915–2922. doi: 10.1099/0022-1317-71-12-2915.
    1. Chen WR, Rico-Hesse R, Tesh RB. A new genotype of Japanese encephalitis virus from Indonesia. Am J Trop Med Hyg. 1992;14:61–69.
    1. Uchil PD, Satchidanandam V. Phylogenetic analysis of Japanese encephalitis virus: envelope gene based analysis reveals a fifth genotype, geographic clustering, and multiple introductions of the virus into the Indian subcontinent. Am J Trop Med Hyg. 2001;14(3):242–251.
    1. Oya A. Japanese Encephalitis Vaccine. Acta Paediatr Jpn. 1988;14:175–184. doi: 10.1111/j.1442-200X.1988.tb02516.x.
    1. Hombach J, Solomon T, Kurane I, Jacobson J, Wood D. Report on a WHO consultation on immunological endpoints for evaluation of new Japanese encephalitis vaccines, WHO, Geneva. 2–3 September 2004. Vaccine. 2005;14(45):5205–5211. doi: 10.1016/j.vaccine.2005.07.002.
    1. Van Gessel Y, Klade CS, Putnak R, Formica A, Krasesub S, Spruth M, Cena B, Tungtaeng A, Gettayacamin M, Dewasthaly S. Correlation of protection against Japanese encephalitis virus and JE vaccine (IXIARO) induced neutralizing antibody titers. Vaccine. 2011;14(35):5925–5931. doi: 10.1016/j.vaccine.2011.06.062.
    1. Reisler RB, Danner DK, Gibbs PH. Immunogenicity of an inactivated Japanese encephalitis vaccine (JE-VAX) in humans over 20 years at USAMRIID: using PRNT50 as an endpoint for immunogenicity. Vaccine. 2010;14:2436–2441. doi: 10.1016/j.vaccine.2009.12.080.
    1. Schuller E, Jilma B, Voicu V, Golor G, Kollaritsch H, Kaltenbock A, Klade C, Tauber E. Long-term immunogenicity of the new Vero cell-derived, inactivated Japanese encephalitis virus vaccine IC51 six and 12 month results of a multicenter follow-up phase 3 study. Vaccine. 2008;14:4382–4386. doi: 10.1016/j.vaccine.2008.05.081.
    1. Fulmali PV, Sapkal GN, Athawale S, Gore MM, Mishra AC, Bondre VP. Introduction of Japanese Encephalitis Virus Genotype I, India. Emerg Infect Dis. 2011;14:319–321. doi: 10.3201/eid1702.100815.
    1. Ma SP, Yoshida Y, Makino Y, Tadano M, Ono T, Ogawa M. A major genotype of Japanese encephalitis virus currently circulating in Japan. Am J Trop Med Hyg. 2003;14:151–154.
    1. Zhang JS, Zhao QM, Guo XF, Zuo SQ, Cheng JX, Jia N, Wu C, Dai PF, Zhao JY. Isolation and genetic characteristics of human genotype 1 Japanese encephalitis virus, China, 2009. PLoS One. 2011;14(1):e16418. doi: 10.1371/journal.pone.0016418.
    1. Erra EO, Askling HH, Yoksan S, Rombo L, Riutta J, Vene S, Lindquist L, Vapalahti O, Kantele A. Cross-Protective Capacity of Japanese Encephalitis (JE) Vaccines Against Circulating Heterologous JE Virus Genotypes. Clin Infect Dis. 2013;14:267–270. doi: 10.1093/cid/cis883.
    1. Fan YC, Chen JM, Chiu HC, Chen YF, Lin JW, Shih CC, Chen CM, Chang CC, Chang GJJ, Chiou SS. Partially neutralizing potency against emerging genotype I virus among children received formalin-inactivated Japanese encephalitis virus vaccine. PLoS Negl Trop Dis. 2012;14(9):e1834. doi: 10.1371/journal.pntd.0001834.
    1. Feroldi E, Pancharoen C, Kosalaraksa P, Watanaveeradej V, Phirangkul K, Capeding MR, Boaz M, Gailhardu S, Bouckenooghe A. Single-dose, live-attenuated Japanese encephalitis vaccine in children aged 12–18 months: randomized, controlled phase 3 immunogenicity and safety trial. Hum Vaccin Immunother. 2012;14:929–937. doi: 10.4161/hv.20071.
    1. Chambers TJ, Nestorowicz A, Mason PW, Rice CM. Yellow fever/Japanese encephalitis chimeric viruses: construction and biological properties. J Virol. 1999;14:3095–3101.
    1. WHO Expert Committee on Biological Standardization. WHO Technical Report Series 910, Annex 3. Geneva: World Health Organization; 2002. pp. 66–98. (Fifty-second report).
    1. Jia L, Wang Z, Yu Y. Protection of SA14-14-2 live attenuated Japanese encephalitis vaccine against the wild-type JE viruses. Chin Med J (Engl) 2003;14:941–943.
    1. Mason PW, Dalrymple JM, Gentry MK, McCown JM, Hoke CH, Burke DS, Fournier MJ, Mason TL. Molecular characterization of a neutralizing domain of the Japanese encephalitis virus structural glycoprotein. J Gen Virol. 1989;14:2037–2049. doi: 10.1099/0022-1317-70-8-2037.
    1. Shimoda H, Mahmoud HYAH, Noguchi K, Terada Y, Takasaki T, Shimojima M, Maeda K. Production and characterization of monoclonal antibodies to Japanese encephalitis virus. J Vet Med Sci. 2013;14:1077–1080. doi: 10.1292/jvms.12-0558.
    1. Kurane I, Takasaki T. Immunogenicity and protective efficacy of the current inactivated Japanese encephalitis vaccine against different Japanese encephalitis virus strains. Vaccine. 2000;14:33–35.
    1. Chen YY, Fan YC, Tu WC, Chang RY, Shih CC, Lu IH, Chien MS, Lee WC, Chen TH, Chang GJ, Chiou SS. Japanese encephalitis virus genotype replacement, Taiwan, 2009–2010. Emerg Infect Dis. 2011;14:2354–2356. doi: 10.3201/eid1712.110914.
    1. Pan XL, Liu H, Wang HY, Fu SH, Liu ZH, Zhang HL, Li MH, Gao XY, Wang JL, Sun XH, Lu XJ, Zhai YG, Meng WS, He Y, Wang HQ, Han N, Wei B, Wu YG, Feng Y, Yang DJ, Wang LH, Tang Q, Xia G, Kurane I, Rayner S, Liang GD. Emergence of genotype I of Japanese encephalitis virus as the dominant genotype in Asia. J Virol. 2011;14:9847–9853. doi: 10.1128/JVI.00825-11.
    1. Sarkar A, Banik BK, Mukhopadhyay SK, Chatterjee S. Envelope protein gene based molecular characterization of Japanese encephalitis virus clinical isolates from West Bengal, India: a comparative approach with respect to SA14-14-2 live attenuated vaccine strain. BMC Infect Dis. 2013;14:368–381. doi: 10.1186/1471-2334-13-368.

Source: PubMed

3
Abonnere