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

Flor M Munoz; Christine M Posavad; Barbra A Richardson; Martina L Badell; Katherine E Bunge; Mark J Mulligan; Lalitha Parameswaran; Clifton W Kelly; Courtney Olson-Chen; Richard M Novak; Rebecca C Brady; Marcela F Pasetti; Emily A Defranco; Jeffrey S Gerber; Mallory C Shriver; Mehul S Suthar; Rhea N Coler; Bryan J Berube; So Hee Kim; Jeanna M Piper; Ashley M Miller; Cristina V Cardemil; Kathleen M Neuzil; Richard H Beigi; DMID 21-0004 Study Group

doi:10.1016/j.vaccine.2023.06.032

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

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

Authors

Flor M Munoz¹, Christine M Posavad², Barbra A Richardson³, Martina L Badell⁴, Katherine E Bunge⁵, Mark J Mulligan⁶, Lalitha Parameswaran⁷, Clifton W Kelly⁸, Courtney Olson-Chen⁹, Richard M Novak¹⁰, Rebecca C Brady¹¹, Marcela F Pasetti¹², Emily A Defranco¹³, Jeffrey S Gerber¹⁴, Mallory C Shriver¹⁵, Mehul S Suthar¹⁶, Rhea N Coler¹⁷, Bryan J Berube¹⁸, So Hee Kim¹⁹, Jeanna M Piper²⁰, Ashley M Miller²¹, Cristina V Cardemil²², Kathleen M Neuzil²³, Richard H Beigi²⁴; DMID 21-0004 Study Group

Affiliations

¹ Departments of Pediatrics and Molecular Virology & Microbiology, Baylor College of Medicine, and Texas Children's Hospital, Houston, TX 77030, United States. Electronic address: florm@bcm.edu.
² Vaccine and Infectious Disease Division, Fred Hutchinson Cancer Center, Department of Laboratory Medicine and Pathology, University of Washington, Seattle, WA 98109, United States. Electronic address: cposavad@fredhutch.org.
³ Vaccine and Infectious Disease Division, Fred Hutchinson Cancer Center, Department of Laboratory Medicine and Pathology, University of Washington, Seattle, WA 98109, United States; Departments of Biostatistics and Global Health, University of Washington, Vaccine and Infectious Disease and Public Health Sciences Divisions, Fred Hutchinson Cancer Center, Seattle, WA 98109, United States. Electronic address: barbrar@uw.edu.
⁴ Department of Gynecology and Obstetrics, Division of Maternal Fetal Medicine, Emory University Hospital Midtown Perinatal Center, Atlanta, GA 30308, United States. Electronic address: mbadell@emory.edu.
⁵ Department of Obstetrics, Gynecology and Reproductive Sciences, UPMC Magee-Womens Hospital, Pittsburgh, PA 15213, United States. Electronic address: bungke@upmc.edu.
⁶ NYU Langone Vaccine Center and Division of Infectious Diseases and Immunology, Department of Medicine, NYU Grossman School of Medicine, New York, NY 10016, United States. Electronic address: mark.mulligan@nyulangone.org.
⁷ NYU Langone Vaccine Center and Division of Infectious Diseases and Immunology, Department of Medicine, NYU Grossman School of Medicine, New York, NY 10016, United States. Electronic address: lalitha.parameswaran@nyulangone.org.
⁸ Statistical Center for HIV/AIDS Research and Prevention (SCHARP), Fred Hutchinson Cancer Center, Seattle, WA 98109, United States. Electronic address: cwkelly@scharp.org.
⁹ Department of Obstetrics and Gynecology, University of Rochester, Rochester, NY 14642, United States. Electronic address: courtney_olson-chen@urmc.rochester.edu.
¹⁰ Division of Infectious Diseases, University of Illinois, Chicago, IL 60612, United States. Electronic address: rmnovak@uic.edu.
¹¹ Cincinnati Children's Hospital Medical Center, Division of Infectious Diseases, University of Cincinnati College of Medicine, Cincinnati, OH 45229, United States. Electronic address: rebecca.brady@cchmc.org.
¹² Center for Vaccine Development and Global Health, University of Maryland School of Medicine, Baltimore, MD 21201, United States. Electronic address: mpasetti@som.umaryland.edu.
¹³ Cincinnati Children's Hospital Medical Center, Division of Infectious Diseases, University of Cincinnati College of Medicine, Cincinnati, OH 45229, United States. Electronic address: defranee@ucmail.uc.edu.
¹⁴ Division of Infectious Diseases, Children's Hospital of Philadelphia, University of Pennsylvania Perelman School of Medicine, Philadelphia, PA 19146, United States. Electronic address: gerberj@chop.edu.
¹⁵ Center for Vaccine Development and Global Health, University of Maryland School of Medicine, Baltimore, MD 21201, United States. Electronic address: mallory.shriver@som.umaryland.edu.
¹⁶ Emory Vaccine Center, Yerkes National Primate Research Center, Department of Microbiology and Immunology, Emory School of Medicine, Emory University, Atlanta, GA 30322, United States. Electronic address: mehul.s.suthar@emory.edu.
¹⁷ Seattle Children's Research Institute, Center for Global Infectious Disease Research, Seattle, WA 98109, United States. Electronic address: Rhea.Coler@seattlechildrens.org.
¹⁸ Seattle Children's Research Institute, Center for Global Infectious Disease Research, Seattle, WA 98109, United States. Electronic address: Bryan.Berube@seattlechildrens.org.
¹⁹ Statistical Center for HIV/AIDS Research and Prevention (SCHARP), Fred Hutchinson Cancer Center, Seattle, WA 98109, United States. Electronic address: skim234@scharp.org.
²⁰ National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, MD 20850, United States. Electronic address: piperj@niaid.nih.gov.
²¹ FHI 360, Durham, NC 27701, United States. Electronic address: amiller@fhi360.org.
²² National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, MD 20850, United States. Electronic address: cristina.cardemil@nih.gov.
²³ Center for Vaccine Development and Global Health, University of Maryland School of Medicine, Baltimore, MD 21201, United States. Electronic address: kneuzil@som.umaryland.edu.
²⁴ Department of Obstetrics, Gynecology and Reproductive Sciences, UPMC Magee-Womens Hospital, Pittsburgh, PA 15213, United States. Electronic address: beigrh@upmc.edu.

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.

Publication types

Multicenter Study

MeSH terms

Antibodies, Blocking
Antibodies, Neutralizing
Antibodies, Viral
COVID-19 Vaccines
COVID-19* / prevention & control
Cohort Studies
Female
Humans
Infant, Newborn
Pregnancy
Pregnancy Complications, Infectious* / prevention & control
Prospective Studies
SARS-CoV-2
Vaccination

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

Authors

Affiliations

Abstract

Publication types

MeSH terms

Substances

Supplementary concepts

Grants and funding