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Pre-Omicron Vaccine Breakthrough Infection Induces Superior Cross-Neutralization against SARS-CoV-2 Omicron BA.1 Compared to Infection Alone.
Int J Mol Sci. 2022 Jul 12; 23(14)IJ

Abstract

SARS-CoV-2 variants raise concern because of their high transmissibility and their ability to evade neutralizing antibodies elicited by prior infection or by vaccination. Here, we compared the neutralizing abilities of sera from 70 unvaccinated COVID-19 patients infected before the emergence of variants of concern (VOCs) and of 16 vaccine breakthrough infection (BTI) cases infected with Gamma or Delta against the ancestral B.1 strain, the Gamma, Delta and Omicron BA.1 VOCs using live virus. We further determined antibody levels against the Nucleocapsid (N) and full Spike proteins, the receptor-binding domain (RBD) and the N-terminal domain (NTD) of the Spike protein. Convalescent sera featured considerable variability in the neutralization of B.1 and in the cross-neutralization of different strains. Their neutralizing capacity moderately correlated with antibody levels against the Spike protein and the RBD. All but one convalescent serum failed to neutralize Omicron BA.1. Overall, convalescent sera from patients with moderate disease had higher antibody levels and displayed a higher neutralizing ability against all strains than patients with mild or severe forms of the disease. The sera from BTI cases fell into one of two categories: half the sera had a high neutralizing activity against the ancestral B.1 strain as well as against the infecting strain, while the other half had no or a very low neutralizing activity against all strains. Although antibody levels against the spike protein and the RBD were lower in BTI sera than in unvaccinated convalescent sera, most neutralizing sera also retained partial neutralizing activity against Omicron BA.1, suggestive of a better cross-neutralization and higher affinity of vaccine-elicited antibodies over virus-induced antibodies. Accordingly, the IC50: antibody level ratios were comparable for BTI and convalescent sera, but remained lower in the neutralizing convalescent sera from patients with moderate disease than in BTI sera. The neutralizing activity of BTI sera was strongly correlated with antibodies against the Spike protein and the RBD. Together, these findings highlight qualitative differences in antibody responses elicited by infection in vaccinated and unvaccinated individuals. They further indicate that breakthrough infection with a pre-Omicron variant boosts immunity and induces cross-neutralizing antibodies against different strains, including Omicron BA.1.

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Authors+Show Affiliations

da Silva ES
HIV Clinical and Translational Research Unit, Department of Infection and Immunity, Luxembourg Institute of Health, 29 rue Henri Koch, L-4354 Esch-sur-Alzette, Luxembourg.
Kohnen M
Centre Hospitalier de Luxembourg, 4 rue Ernest Barblé, L-1210 Luxembourg, Luxembourg.
Gilson G
Centre Hospitalier de Luxembourg, 4 rue Ernest Barblé, L-1210 Luxembourg, Luxembourg.
Staub T
Centre Hospitalier de Luxembourg, 4 rue Ernest Barblé, L-1210 Luxembourg, Luxembourg.
Arendt V
Centre Hospitalier de Luxembourg, 4 rue Ernest Barblé, L-1210 Luxembourg, Luxembourg.
Hilger C
Molecular and Translational Allergology, Department of Infection and Immunity, Luxembourg Institute of Health, 29 rue Henri Koch, L-4354 Esch-sur-Alzette, Luxembourg.
Servais JY
HIV Clinical and Translational Research Unit, Department of Infection and Immunity, Luxembourg Institute of Health, 29 rue Henri Koch, L-4354 Esch-sur-Alzette, Luxembourg.
Charpentier E
Clinical and Applied Virology, Department of Infection and Immunity, Luxembourg Institute of Health, 29 rue Henri Koch, L-4354 Esch-sur-Alzette, Luxembourg.
Domingues O
Allergy and Clinical Immunology, Department of Infection and Immunity, Luxembourg Institute of Health, 29 rue Henri Koch, L-4354 Esch-sur-Alzette, Luxembourg.
Snoeck CJ
Clinical and Applied Virology, Department of Infection and Immunity, Luxembourg Institute of Health, 29 rue Henri Koch, L-4354 Esch-sur-Alzette, Luxembourg.
Ollert M
Allergy and Clinical Immunology, Department of Infection and Immunity, Luxembourg Institute of Health, 29 rue Henri Koch, L-4354 Esch-sur-Alzette, Luxembourg.
Seguin-Devaux C
HIV Clinical and Translational Research Unit, Department of Infection and Immunity, Luxembourg Institute of Health, 29 rue Henri Koch, L-4354 Esch-sur-Alzette, Luxembourg.
Perez-Bercoff D
HIV Clinical and Translational Research Unit, Department of Infection and Immunity, Luxembourg Institute of Health, 29 rue Henri Koch, L-4354 Esch-sur-Alzette, Luxembourg.

MeSH

Antibodies, NeutralizingAntibodies, ViralCOVID-19HumansImmunization, PassiveNeutralization TestsSARS-CoV-2Spike Glycoprotein, CoronavirusVaccinesCOVID-19 Serotherapy

Pub Type(s)

Journal Article

Language

eng

PubMed ID

35887023

Citation

da Silva, Eveline Santos, et al. "Pre-Omicron Vaccine Breakthrough Infection Induces Superior Cross-Neutralization Against SARS-CoV-2 Omicron BA.1 Compared to Infection Alone." International Journal of Molecular Sciences, vol. 23, no. 14, 2022.
da Silva ES, Kohnen M, Gilson G, et al. Pre-Omicron Vaccine Breakthrough Infection Induces Superior Cross-Neutralization against SARS-CoV-2 Omicron BA.1 Compared to Infection Alone. Int J Mol Sci. 2022;23(14).
da Silva, E. S., Kohnen, M., Gilson, G., Staub, T., Arendt, V., Hilger, C., Servais, J. Y., Charpentier, E., Domingues, O., Snoeck, C. J., Ollert, M., Seguin-Devaux, C., & Perez-Bercoff, D. (2022). Pre-Omicron Vaccine Breakthrough Infection Induces Superior Cross-Neutralization against SARS-CoV-2 Omicron BA.1 Compared to Infection Alone. International Journal of Molecular Sciences, 23(14). https://doi.org/10.3390/ijms23147675
da Silva ES, et al. Pre-Omicron Vaccine Breakthrough Infection Induces Superior Cross-Neutralization Against SARS-CoV-2 Omicron BA.1 Compared to Infection Alone. Int J Mol Sci. 2022 Jul 12;23(14) PubMed PMID: 35887023.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Pre-Omicron Vaccine Breakthrough Infection Induces Superior Cross-Neutralization against SARS-CoV-2 Omicron BA.1 Compared to Infection Alone. AU - da Silva,Eveline Santos, AU - Kohnen,Michel, AU - Gilson,Georges, AU - Staub,Therese, AU - Arendt,Victor, AU - Hilger,Christiane, AU - Servais,Jean-Yves, AU - Charpentier,Emilie, AU - Domingues,Olivia, AU - Snoeck,Chantal J, AU - Ollert,Markus, AU - Seguin-Devaux,Carole, AU - Perez-Bercoff,Danielle, Y1 - 2022/07/12/ PY - 2022/06/17/received PY - 2022/07/08/revised PY - 2022/07/09/accepted PY - 2022/7/27/entrez PY - 2022/7/28/pubmed PY - 2022/7/29/medline KW - Delta KW - Omicron BA.1 KW - SARS-CoV-2 KW - breakthrough infection KW - convalescent sera KW - neutralizing antibodies KW - variants of concern (VOCs) JF - International journal of molecular sciences JO - Int J Mol Sci VL - 23 IS - 14 N2 - SARS-CoV-2 variants raise concern because of their high transmissibility and their ability to evade neutralizing antibodies elicited by prior infection or by vaccination. Here, we compared the neutralizing abilities of sera from 70 unvaccinated COVID-19 patients infected before the emergence of variants of concern (VOCs) and of 16 vaccine breakthrough infection (BTI) cases infected with Gamma or Delta against the ancestral B.1 strain, the Gamma, Delta and Omicron BA.1 VOCs using live virus. We further determined antibody levels against the Nucleocapsid (N) and full Spike proteins, the receptor-binding domain (RBD) and the N-terminal domain (NTD) of the Spike protein. Convalescent sera featured considerable variability in the neutralization of B.1 and in the cross-neutralization of different strains. Their neutralizing capacity moderately correlated with antibody levels against the Spike protein and the RBD. All but one convalescent serum failed to neutralize Omicron BA.1. Overall, convalescent sera from patients with moderate disease had higher antibody levels and displayed a higher neutralizing ability against all strains than patients with mild or severe forms of the disease. The sera from BTI cases fell into one of two categories: half the sera had a high neutralizing activity against the ancestral B.1 strain as well as against the infecting strain, while the other half had no or a very low neutralizing activity against all strains. Although antibody levels against the spike protein and the RBD were lower in BTI sera than in unvaccinated convalescent sera, most neutralizing sera also retained partial neutralizing activity against Omicron BA.1, suggestive of a better cross-neutralization and higher affinity of vaccine-elicited antibodies over virus-induced antibodies. Accordingly, the IC50: antibody level ratios were comparable for BTI and convalescent sera, but remained lower in the neutralizing convalescent sera from patients with moderate disease than in BTI sera. The neutralizing activity of BTI sera was strongly correlated with antibodies against the Spike protein and the RBD. Together, these findings highlight qualitative differences in antibody responses elicited by infection in vaccinated and unvaccinated individuals. They further indicate that breakthrough infection with a pre-Omicron variant boosts immunity and induces cross-neutralizing antibodies against different strains, including Omicron BA.1. SN - 1422-0067 UR - https://www.unboundmedicine.com/medline/citation/35887023/Pre_Omicron_Vaccine_Breakthrough_Infection_Induces_Superior_Cross_Neutralization_against_SARS_CoV_2_Omicron_BA_1_Compared_to_Infection_Alone_ DB - PRIME DP - Unbound Medicine ER -