The effect of maternal poliovirus antibodies on the immune responses of infants to poliovirus vaccines

Siyue Jia, Rong Tang, Guifan Li, Yuemei Hu, Qi Liang, Siyue Jia, Rong Tang, Guifan Li, Yuemei Hu, Qi Liang

Abstract

Background: Maternal poliovirus antibodies could provide passive immunity to the newborns from poliovirus infection during their first few months of life, but they may impair the immune responses of infants to the poliovirus vaccine as well. In our study, we pooled the data from three clinical trials of the inactivated poliovirus vaccine (IPV) based on Sabin strains to investigate the effect of maternal poliovirus antibodies on the immune responses of infants to poliovirus vaccines.

Methods: There were five groups in the pooled analysis, including low-dose Sabin IPV, medium-dose Sabin IPV, high-dose Sabin IPV, control Sabin IPV, and control Salk IPV groups. We reclassified the infants in different groups according to their maternal poliovirus antibodies by two methods, the first one included maternal antibody negative (< 1:8) and maternal antibody positive (≥1:8), and the second one included maternal antibody titer < 1:8, 1:8 ~ < 1:32 and ≥ 1:32. Then, we compared the geometric mean titers (GMTs), geometric mean antibody fold increases (GMIs) and seroconversion rates of poliovirus type-specific neutralizing antibodies after vaccination among participants with different maternal poliovirus antibody levels.

Results: The GMTs and GMIs of three types of poliovirus antibodies after vaccination in maternal antibody negative participants were significantly higher than those in maternal antibody positive participants. The seroconversion rates of type II and type III poliovirus antibodies in maternal antibody positive participants were significantly lower than those in maternal antibody negative participants. Among participants with maternal antibody titer < 1:8, 1:8 ~ < 1:32 and ≥ 1:32, the GMTs and GMIs of three types of poliovirus antibodies after vaccination showed a tendency to decline with the increasing of maternal antibody levels. The seroconversion rates of three types of poliovirus antibodies in participants with maternal antibody titer ≥1:32 were significantly lower than those in participants with maternal antibody titer < 1:8 and 1:8 ~ < 1:32.

Conclusions: Maternal poliovirus antibodies interfered with the immune responses of infants to poliovirus vaccines, and a high level of maternal antibodies exhibited a greater dampening effect.

Trial registration: ClinicalTrials.gov NCT04264598 February 11, 2020; ClinicalTrials.gov NCT04264546 February 11, 2020; ClinicalTrials.gov NCT03902054 April 3, 2019. Retrospectively registered.

Keywords: Immune response; Maternal antibody; Poliovirus vaccine.

Conflict of interest statement

Guifan Li is an employee of Beijing Minhai Biotechnology Co., Ltd. The authors have no other relevant affiliations or financial involvement with any organization or entity with a financial interest in or financial conflict with the subject matter or materials discussed in the manuscript apart from those disclosed.

Figures

Fig. 1
Fig. 1
Pooled analysis profile
Fig. 2
Fig. 2
Multiple comparisons of GMTs, GMIs and seroconversion rates of poliovirus type-specific neutralizing antibodies after vaccination among participants with different maternal poliovirus antibody levels. Group 1: low-dose Sabin IPV group. Group 2: medium-dose Sabin IPV group. Group 3: high-dose Sabin IPV group. Group 4: control Sabin IPV group. Group 5: control Salk IPV group

References

    1. World Health Organization. Polio eradication. . Accessed 10 Jan 2020.
    1. World Health Organization. Two out of three wild poliovirus strains eradicated. . Accessed 15 Jan 2020.
    1. World Health Organization. Global Polio Eradication Initiative. . Accessed 2 Feb 2020.
    1. Heinsbroek E, Ruitenberg EJ. The global introduction of inactivated polio vaccine can circumvent the oral polio vaccine paradox. Vaccine. 2010;28(22):3778–3783. doi: 10.1016/j.vaccine.2010.02.095.
    1. Centers for Disease Control and Prevention. What are the Types of Polio Vaccine? . Accessed 10 Feb 2020.
    1. Liao G, Li R, Li C, Sun M, Li Y, Chu J, Jiang S, Li Q. Safety and immunogenicity of inactivated poliovirus vaccine made from Sabin strains: a phase II, randomized, positive-controlled trial. J Infect Dis. 2012;205(2):237–243. doi: 10.1093/infdis/jir723.
    1. Verdijk P, Rots NY, van Oijen MGCT, Oberste MS, Boog CJ, Okayasu H, Sutter RW, Bakker WAM. Safety and immunogenicity of inactivated poliovirus vaccine based on Sabin strains with and without aluminum hydroxide: a phase I trial in healthy adults. Vaccine. 2013;31(47):5531–5536. doi: 10.1016/j.vaccine.2013.09.021.
    1. Vojtek I, Dieussaert I, Doherty TM, Franck V, Hanssens L, Miller J, Bekkat-Berkani R, Kandeil W, Prado-Cohrs D, Vyse A. Maternal immunization: where are we now and how to move forward? Ann Med. 2018;50(3):193–208. doi: 10.1080/07853890.2017.1421320.
    1. Albrecht P, Ennis FA, Saltzman EJ, Krugman S. Persistence of maternal antibody in infants beyond 12 months: mechanism of measles vaccine failure. J Pediatr. 1977;91(5):715–718. doi: 10.1016/S0022-3476(77)81021-4.
    1. Letson GW, Shapiro CN, Kuehn D, Gardea C, Welty TK, Krause DS, Lambert SB, Margolis HS. Effect of maternal antibody on immunogenicity of hepatitis A vaccine in infants. J Pediatr. 2004;144(3):327–332. doi: 10.1016/j.jpeds.2003.11.030.
    1. Hu Y, Wu Q, Xu B, Zhou Z, Wang Z, Zhou Y-H. Influence of maternal antibody against hepatitis B surface antigen on active immune response to hepatitis B vaccine in infants. Vaccine. 2008;26(48):6064–6067. doi: 10.1016/j.vaccine.2008.09.014.
    1. Voysey M, Kelly DF, Fanshawe TR, Sadarangani M, O'Brien KL, Perera R, Pollard AJ. The influence of maternally derived antibody and infant age at vaccination on infant vaccine responses: an individual participant meta-analysis. JAMA Pediatr. 2017;171(7):637–646. doi: 10.1001/jamapediatrics.2017.0638.
    1. Asturias E, Dueger E, Omer S, Melville A, Nates S, Laassri M, Chumakov K, Halsey N. Randomized trial of inactivated and live polio vaccine schedules in Guatemalan infants. J Infect Dis. 2007;196(5):692–698. doi: 10.1086/520546.
    1. Dayan G, Thorley M, Yamamura Y, Rodríguez N, McLaughlin S, Torres L, Seda A, Carbia M, Alexander L, Caceres V. Serologic response to inactivated poliovirus vaccine: a randomized clinical trial comparing 2 vaccination schedules in Puerto Rico. J Infect Dis. 2007;195(1):12–20. doi: 10.1086/508427.
    1. Sormunen H, Stenvik M, Eskola J, Hovi T. Age- and dose-interval-dependent antibody responses to inactivated poliovirus vaccine. J Med Virol. 2001;63(4):305–310. doi: 10.1002/1096-9071(200104)63:4<305::AID-JMV1006>;2-U.
    1. Linder N, Handsher R, German B, Sirota L, Bachman M, Zinger S, Mendelson E, Barzilai A. Controlled trial of immune response of preterm infants to recombinant hepatitis B and inactivated poliovirus vaccines administered simultaneously shortly after birth. Arch Dis Child Fetal Neonatal Ed. 2000;83(1):F24–F27. doi: 10.1136/fn.83.1.F24.
    1. World Health Organization. Manual for the virological investigation of polio. . Accessed 24 Nov 2011.
    1. Hu Y, Xu K, Han W, Chu K, Jiang D, Wang J, Tian X, Ying Z, Zhang Y, Li C, et al. Safety and Immunogenicity of Sabin Strain Inactivated Poliovirus Vaccine Compared With Salk Strain Inactivated Poliovirus Vaccine, in Different Sequential Schedules With Bivalent Oral Poliovirus Vaccine: Randomized Controlled Noninferiority Clinical Trials in China. Open Forum Infect Dis. 2019;6(10):ofz380. doi: 10.1093/ofid/ofz380.
    1. Tang R, Chu K, Hu Y, Chen L, Zhang M, Liu S, Ma H, Wang J, Zhu F, Hu Y, et al. Effect of maternal antibody on the infant immune response to inactivated poliovirus vaccines made from Sabin strains. Hum Vaccin Immunother. 2019;15(5):1160–1166. doi: 10.1080/21645515.2019.1572410.
    1. Adams A, Boualam L, Diorditsa S, Gregory C, Jee Y, Mendoza-Aldana J, Roesel S. Maintaining polio-free certification in the World Health Organization Western Pacific region for over a decade. J Infect Dis. 2014;210(suppl 1):S259–S267. doi: 10.1093/infdis/jiu164.
    1. Jia S, Li J, Liu Y, Zhu F. Precision immunization: a new trend in human vaccination. Hum Vaccin Immunother. 2020:1–10.

Source: PubMed

Sponsor e collaboratori

Condizioni mediche

Interventi farmacologici

3
Sottoscrivi