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Figure.  Persistence of Antibody in Infants After Maternal COVID-19 Vaccination or Infection
Persistence of Antibody in Infants After Maternal COVID-19 Vaccination or Infection

Black lines represent the median for each group at each time point. Differences in titer between groups at birth and the 6-month time points were assessed by Mann-Whitney U test. Due to the timing of COVID-19 cases relative to the study period, infants born to mothers infected with COVID-19 during pregnancy were older than 2 months at sample collection (see eMethods in the Supplement). OD450-570 indicates optical density at 450 nm corrected from a reference wavelength of 570 nm. Detectable anti-spike IgG was defined as any value greater than the sum of the mean value of assay negative controls (SARS-CoV-2–negative, unvaccinated samples) and 3 times the standard deviation of those samples.

Table.  Demographic and Clinical Data for Participants Vaccinated Against COVID-19 vs Those With Natural COVID-19 Infection
Demographic and Clinical Data for Participants Vaccinated Against COVID-19 vs Those With Natural COVID-19 Infection
1.
Gray  KJ, Bordt  EA, Atyeo  C,  et al.  Coronavirus disease 2019 vaccine response in pregnant and lactating women: a cohort study.   Am J Obstet Gynecol. 2021;225(3):303-303. doi:10.1016/j.ajog.2021.03.023PubMedGoogle ScholarCrossref
2.
Prabhu  M, Murphy  EA, Sukhu  AC,  et al.  Antibody response to coronavirus disease 2019 (COVID-19) messenger RNA vaccination in pregnant women and transplacental passage into cord blood.   Obstet Gynecol. 2021;138(2):278-280. doi:10.1097/AOG.0000000000004438PubMedGoogle Scholar
3.
Beharier  O, Plitman Mayo  R, Raz  T,  et al.  Efficient maternal to neonatal transfer of antibodies against SARS-CoV-2 and BNT162b2 mRNA COVID-19 vaccine.   J Clin Invest. 2021;131(13):e150319. doi:10.1172/JCI150319PubMedGoogle Scholar
4.
Mithal  LB, Otero  S, Shanes  ED, Goldstein  JA, Miller  ES.  Cord blood antibodies following maternal coronavirus disease 2019 vaccination during pregnancy.   Am J Obstet Gynecol. 2021;225(2):192-194. doi:10.1016/j.ajog.2021.03.035PubMedGoogle ScholarCrossref
5.
Yang  YJ, Murphy  EA, Singh  S,  et al.  Association of gestational age at coronavirus disease 2019 (COVID-19) vaccination, history of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection, and a vaccine booster dose with maternal and umbilical cord antibody levels at delivery.   Obstet Gynecol. Published online December 28, 2021. doi:10.1097/AOG.0000000000004693PubMedGoogle Scholar
6.
Dong  Y, Mo  X, Hu  Y,  et al.  Epidemiology of COVID-19 among children in China.   Pediatrics. 2020;145(6):e20200702. doi:10.1542/peds.2020-0702PubMedGoogle Scholar
Research Letter
February 7, 2022

Durability of Anti-Spike Antibodies in Infants After Maternal COVID-19 Vaccination or Natural Infection

Author Affiliations
  • 1Department of Obstetrics & Gynecology, Massachusetts General Hospital, Boston
  • 2Ragon Institute of MGH, MIT, and Harvard, Cambridge, Massachusetts
  • 3Department of Pediatrics, Massachusetts General Hospital, Boston
  • 4Department of Obstetrics & Gynecology, Brigham and Women’s Hospital, Boston, Massachusetts
JAMA. 2022;327(11):1087-1089. doi:10.1001/jama.2022.1206

COVID-19 vaccination in pregnancy generates functional anti-spike (anti-S) IgG antibodies in maternal circulation that are detectable in umbilical cord blood at birth and can protect newborns and infants from COVID-19.1-4 Anti-S IgG titers in the umbilical cord are correlated with maternal titers and are highest after late second and early third trimester vaccination.2-4 We characterized the persistence of vaccine-induced maternal anti-S IgG in infant blood and compared persistence of infant anti-S IgG after maternal vaccination vs natural infection.

Methods

The study included individuals who had received an mRNA COVID-19 vaccine in pregnancy or were infected with SARS-CoV-2 at 20 to 32 weeks’ gestation, had enrolled in a prospective study at 2 academic medical centers in Boston, and had enrolled their infants in this follow-up study conducted from July 21, 2021, to October 22, 2021. Individuals vaccinated or infected at 20 to 32 weeks’ gestation were enrolled because previous studies have demonstrated superior transplacental transfer of antibodies during this window compared with vaccination closer to delivery.4,5 Those infected before vaccination were excluded. Matched maternal and umbilical cord serum samples were collected at birth. Infant capillary serum samples were collected via microneedle device at 2 months after birth for infants of vaccinated mothers and at 6 months for infants of mothers who were vaccinated and mothers who had been infected with SARS-CoV-2. Antibody titers against the SARS-CoV-2 spike protein were quantified using an enzyme-linked immunosorbent assay (eMethods in the Supplement). Differences in titers between vaccinated and infected groups at delivery and 6-month infant age were assessed by the Mann-Whitney U test. Differences in proportions of infants with detectable antibodies at 6 months were assessed by the Fisher exact test. Correlation between delivery titers and infant antibody was assessed via the Spearman rank test. Analyses were conducted using Prism version 9.0. Significance was defined as a 2-sided P < .05. The study was approved by the Mass General Brigham institutional review board, and all participants provided written informed consent.

Results

Seventy-seven vaccinated pregnant mothers and 12 with symptomatic SARS-CoV-2 infection in pregnancy were included (Table). At 2 months, capillary serum samples were collected from 49 infants of vaccinated mothers; at 6 months, serum samples were collected from 28 infants of vaccinated mothers (mean, 170 days after birth) and 12 infants of infected mothers (mean, 207 days after birth).

Vaccinated mothers had significantly higher titers at delivery, with a mean of 2.03 (SD, 0.47) optical density (OD450-570), compared with mothers after infection, with a mean of 0.65 (SD, 0.76) OD450-570 (P < .001). Similarly, the respective mean cord titers were higher after vaccination vs natural infection: 2.17 (SD, 0.50) OD450-570 vs 1.00 (SD, 0.83) OD450-570 (P < .001) (Figure). Among infants of vaccinated mothers at 2 months, 98% (48 of 49) had detectable anti-S IgG. The mean titer at 2 months was 1.29 (SD, 0.53) OD450-570, which was correlated with both maternal (r = 0.55; P < .001) and cord titers (r = 0.43; P = .01) at delivery.

Vaccination resulted in significantly greater antibody persistence in infants than infection. At 6 months, 57% (16 of 28) of infants born to vaccinated mothers had detectable antibodies (Table) compared with 8% (1 of 12) of infants born to infected mothers (P = .005). Titers were a mean of 0.33 (SD, 0.46) OD450-570 among infants of vaccinated mothers and 0 (SD, 0.01) OD450-570 among infants of infected mothers (P = .004) (Figure). Neither maternal (P = .23) nor cord (P = .05) titers were significantly correlated with infant anti-S titers at 6 months, largely because 43% of infants had no detectable titer at that time.

Discussion

This study found that the majority of infants born to COVID-vaccinated mothers had persistent anti-S antibodies at 6 months compared with infants born to mothers with SARS-CoV-2 infection. Understanding the persistence of maternal antibody levels in infants is important because COVID-19 infections in this age group account for a disproportionate burden of pediatric SARS-CoV-2–associated morbidity6 and because COVID-19 vaccines are not currently planned for administration to infants younger than 6 months. Study limitations include the small number of infants, the longer mean time to follow-up in the infected group (due to pragmatic constraints related to timing of COVID-19 surges in Boston and the availability of participants for timely follow-up), and the reporting of antibody titers rather than clinical outcomes. Although the antibody titer known to be protective against COVID-19 in infants is unknown, these findings provide further incentive for pregnant individuals to pursue COVID-19 vaccination.

Section Editors: Jody W. Zylke, MD, Deputy Editor; Kristin Walter, MD, Associate Editor.
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Article Information

Accepted for Publication: January 21, 2022.

Published Online: February 7, 2022. doi:10.1001/jama.2022.1206

Corresponding Author: Andrea G. Edlow, MD, MSc, Department of Obstetrics & Gynecology, Massachusetts General Hospital, 55 Fruit St, Their Bldg, Floor 9, Boston, MA 02114 (aedlow@mgh.harvard.edu).

Author Contributions: Drs Alter and Edlow had full access to all of the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. Dr Shook and Ms Atyeo contributed equally to this work. Drs Alter and Edlow contributed equally to this work.

Concept and design: Yonker, Fasano, Alter, Edlow.

Acquisition, analysis, or interpretation of data: Shook, Atyeo, Yonker, Gray, Alter, Edlow.

Drafting of the manuscript: Shook, Atyeo, Yonker, Alter, Edlow.

Critical revision of the manuscript for important intellectual content: Shook, Atyeo, Yonker, Fasano, Gray, Alter.

Statistical analysis: Shook, Atyeo, Alter, Edlow.

Obtained funding: Fasano, Alter, Edlow.

Administrative, technical, or material support: Yonker, Gray, Alter, Edlow.

Supervision: Yonker, Fasano, Gray, Alter, Edlow.

Conflict of Interest Disclosures: Dr Fasano reported being a cofounder and stockholder of Alba Therapeutics; serving on the scientific advisory board of Viome; and receiving personal fees from Milky Way and Mead Johnson Nutrition. Dr Gray reported receiving nonfinancial support from Illumina, Aetion, and BillionToOne. Dr Alter reported being the founder of and consultant to Systems Seromyx; receiving grants from Sanofi, GlaxoSmithKline, BioNTech, and Medicago; and being a consultant to Leyden Labs. No other disclosures were reported.

Funding/Support: This study was supported by grants 1R01HD100022-01 and 3R01HD100022-02S2 (Dr Edlow) and 1K12HD103096 (Dr Shook) from the National Institute of Child Health and Human Development; grant 6-FY20-223 from the March of Dimes (Dr Edlow); grants K08HL1469630-03 and 3K08HL146963-02S1 (Dr Gray) and 5K08HL143183 (Dr Yonker) from the National Heart, Lung, and Blood Institute; the Ragon Institute of MGH, MIT, and Harvard and the MGH ECOR Scholars award (Dr Alter); the Nancy Zimmerman, Samana Kay MGH Research Scholars award (Dr Alter); grants 3R37AI080289-11S1, R01AI146785, U19AI42790-01, U19AI135995-02, 1U01CA260476-01, and CIVIC5N93019C00052 from the National Institute of Allergy and Infectious Diseases (Dr Alter); and grants OPP1146996 and INV-001650 from the Gates Foundation Global Health Vaccine Accelerator Platform (Dr Alter). The TAPII blood collection devices for infant blood draw were provided at reduced cost by YourBio Health.

Role of the Funder/Sponsor: The sponsors had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication.

Additional Contributions: We thank Madeleine Burns, BS, MS, of the Massachusetts General Hospital Department of Pediatrics, for her contributions to participant recruitment and sample collection. She was not compensated for this work beyond her salary as a clinical research coordinator.

References
1.
Gray  KJ, Bordt  EA, Atyeo  C,  et al.  Coronavirus disease 2019 vaccine response in pregnant and lactating women: a cohort study.   Am J Obstet Gynecol. 2021;225(3):303-303. doi:10.1016/j.ajog.2021.03.023PubMedGoogle ScholarCrossref
2.
Prabhu  M, Murphy  EA, Sukhu  AC,  et al.  Antibody response to coronavirus disease 2019 (COVID-19) messenger RNA vaccination in pregnant women and transplacental passage into cord blood.   Obstet Gynecol. 2021;138(2):278-280. doi:10.1097/AOG.0000000000004438PubMedGoogle Scholar
3.
Beharier  O, Plitman Mayo  R, Raz  T,  et al.  Efficient maternal to neonatal transfer of antibodies against SARS-CoV-2 and BNT162b2 mRNA COVID-19 vaccine.   J Clin Invest. 2021;131(13):e150319. doi:10.1172/JCI150319PubMedGoogle Scholar
4.
Mithal  LB, Otero  S, Shanes  ED, Goldstein  JA, Miller  ES.  Cord blood antibodies following maternal coronavirus disease 2019 vaccination during pregnancy.   Am J Obstet Gynecol. 2021;225(2):192-194. doi:10.1016/j.ajog.2021.03.035PubMedGoogle ScholarCrossref
5.
Yang  YJ, Murphy  EA, Singh  S,  et al.  Association of gestational age at coronavirus disease 2019 (COVID-19) vaccination, history of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection, and a vaccine booster dose with maternal and umbilical cord antibody levels at delivery.   Obstet Gynecol. Published online December 28, 2021. doi:10.1097/AOG.0000000000004693PubMedGoogle Scholar
6.
Dong  Y, Mo  X, Hu  Y,  et al.  Epidemiology of COVID-19 among children in China.   Pediatrics. 2020;145(6):e20200702. doi:10.1542/peds.2020-0702PubMedGoogle Scholar
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