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Multicenter Study
. 2023 Aug 14;41(36):5296-5303.
doi: 10.1016/j.vaccine.2023.06.032. Epub 2023 Jun 13.

COVID-19 booster vaccination during pregnancy enhances maternal binding and neutralizing antibody responses and transplacental antibody transfer to the newborn

Flor M Munoz  1 , Christine M Posavad  2 , Barbra A Richardson  3 , Martina L Badell  4 , Katherine E Bunge  5 , Mark J Mulligan  6 , Lalitha Parameswaran  7 , Clifton W Kelly  8 , Courtney Olson-Chen  9 , Richard M Novak  10 , Rebecca C Brady  11 , Marcela F Pasetti  12 , Emily A Defranco  13 , Jeffrey S Gerber  14 , Mallory C Shriver  15 , Mehul S Suthar  16 , Rhea N Coler  17 , Bryan J Berube  18 , So Hee Kim  19 , Jeanna M Piper  20 , Ashley M Miller  21 , Cristina V Cardemil  22 , Kathleen M Neuzil  23 , Richard H Beigi  24 ; DMID 21-0004 Study Group
Affiliations
Multicenter Study

COVID-19 booster vaccination during pregnancy enhances maternal binding and neutralizing antibody responses and transplacental antibody transfer to the newborn

Flor M Munoz et al. Vaccine. .

Abstract

The immune response to COVID-19 booster vaccinations during pregnancy for mothers and their newborns and the functional response of vaccine-induced antibodies against Omicron variants are not well characterized. We conducted a prospective, multicenter cohort study of participants vaccinated during pregnancy with primary or booster mRNA COVID-19 vaccines from July 2021 to January 2022 at 9 academic sites. We determined SARS-CoV-2 binding and live virus and pseudovirus neutralizing antibody (nAb) titers pre- and post-vaccination, and at delivery for both maternal and infant participants. Immune responses to ancestral and Omicron BA.1 SARS-CoV-2 strains were compared between primary and booster vaccine recipients in maternal sera at delivery and in cord blood, after adjusting for days since last vaccination. A total of 240 participants received either Pfizer or Moderna mRNA vaccine during pregnancy (primary 2-dose series: 167; booster dose: 73). Booster vaccination resulted in significantly higher binding and nAb titers, including to the Omicron BA.1 variant, in maternal serum at delivery and in cord blood compared to a primary 2-dose series (range 0.44-0.88 log10 higher, p < 0.0001 for all comparisons). Live virus nAb to Omicron BA.1 were present at delivery in 9 % (GMT ID50 12.7) of Pfizer and 22 % (GMT ID50 14.7) of Moderna primary series recipients, and in 73 % (GMT ID50 60.2) of mRNA boosted participants (p < 0.0001), although titers were significantly lower than to the D614G strain. Transplacental antibody transfer was efficient for all regimens with median transfer ratio range: 1.55-1.77 for IgG, 1.00-1.78 for live virus nAb and 1.79-2.36 for pseudovirus nAb. COVID-19 mRNA vaccination during pregnancy elicited robust immune responses in mothers and efficient transplacental antibody transfer to the newborn. A booster dose during pregnancy significantly increased maternal and cord blood binding and neutralizing antibody levels, including against Omicron BA.1. Findings support the use of a booster dose of COVID-19 vaccine during pregnancy.

Keywords: Booster vaccination; COVID-19; Neutralizing antibodies; Newborn; Pregnancy; SARS-CoV-2; Transplacental antibody.

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Conflict of interest statement

Declaration of Competing Interest The authors declare the following financial interests/personal relationships which may be considered as potential competing interests: F.M.M. is an investigator of pediatric studies of COVID-19 vaccines for Pfizer and for a pediatric remdesivir study conducted by Gilead Sciences, Inc; serves as investigator on projects supported by an NIH contract for a Vaccine Treatment and Evaluation Unit (VTEU), serves as member of the Data Safety monitoring Board (DSMB) for clinical trials conducted by Pfizer, Moderna, Meissa Vaccines, Virometix, and the NIH; and is a member of the American Academy of Pediatrics Section of Infectious Diseases (SOID), the Immunization Expert Group of the American College of Obstetrics and Gynecology (ACOG), and was co-Chair of the COVAX-CEPI Maternal Immunization Working Group. K.M.N. is a member of the World Health Organization (WHO) Strategic Advisory Group of Experts on Immunization, serves as co-investigator on an NIH contract for a Vaccine Treatment and Evaluation Unit (VTEU), serves as Co-Chair of the NIH COVID Prevention Network (CoVPN), and served as an investigator for Phase I/II Pfizer COVID-19 vaccine grant, with a grant to the institution, but no salary support. M.J.M. conducts laboratory research and clinical trials with contract funding for vaccines or MABs vs SARS-CoV-2 with Lilly, Pfizer, and Sanofi and receives personal fees for Scientific Advisory Board service from Merck, Meissa Vaccines, Inc. and Pfizer. M.S.S. served as an advisor for Moderna (ended December 2021) and is currently serving as an advisor for Ocugen, Inc. B.A.R. currently holds a position on a DSMB for clinical trials at Gilead Sciences, Inc. R.C.B. at Cincinnati Children’s Hospital receives research grant support for clinical trials from PATH, Astra Zeneca and Pfizer on which she serves as co-investigator. B.B. owns shares in HDT Bio Corp. J.S.G. receives research funds from NIH for Moderna KidCOVE study. R.M.N. is a paid advisor to Gilead and an investigator on NIH-funded trials of Moderna, Pfizer and Janssen vaccines. J.R-K is a medical speaker for Abbott Nutrition with the UIC team. A.R.F. holds research grants from Pfizer, Janssen, Merck, Cyanvac, Biofire Diagnostics and serves on the DSMB for Novavax. N.R. receives funds to conduct industry trials from Pfizer, Merck, and Sanofi-Pasteur and serves as a safety consultant for EMMES and ICON. R.W.F. Jr., MD has received funds to conduct industry trials from Pfizer, Moderna and Astra Zeneca, serves on advisory boards for Merck, Sanofi-Pasteur, Johnson and Johnson and Seqirus and serves on an ICON-sponsored DSMB for a C difficile study.

Figures

Figure 1
Figure 1
SARS-CoV-2 binding IgG and pseudovirus nAb activity in maternal and cord blood sera by study group and study visit. Pregnant participants received a 2-dose series of an mRNA vaccine (top – Pfizer, middle – Moderna) or a booster mRNA vaccine (bottom panel). Sera derived from maternal blood collected pre- and post-vaccination and at delivery, and cord blood, were evaluated for binding IgG to full-length Spike (left panels) and RBD (middle panels), or pseudovirus nAb titers (IC50) (right panels). Binding IgG titers were bridged to international standards and reported as Binding Antibody Units (BAU/mL). Box plots represent median (horizontal line within the box) and interquartile range; GMT is displayed at the top of each panel and the dashed line is the cutoff for positivity (17 BAU/mL).
Figure 2
Figure 2
SARS-CoV-2 live virus nAb activity of maternal and cord blood sera by study group and study visit. Pregnant participants received a 2-dose series of an mRNA vaccine (top – Pfizer, middle – Moderna) or a booster mRNA vaccine (bottom panel). Sera derived from maternal blood collected pre- and post-vaccination and at delivery, and cord blood, were evaluated for neutralization of D614G, Delta, and Omicron (BA.1) variants. Each point represents the GMT ID50 from two duplicates per specimen (within the same assay run). A value equivalent to half the lower limit of detection (LLOD = 20) was assigned to observations with no detectable response. A specimen was considered as having a positive response if at least one of the duplicates was above the LLOD. Box plots represent median (horizontal line within the box) and interquartile range. Response rate (% with responses > 20 ID50), GMT, and GMT fold reduction compared to D614G are displayed at the top of each panel.
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