Coronavirus disease 2019 vaccine response in pregnant and lactating women: a cohort study

doi:10.1016/j.ajog.2021.03.023

. 2021 Sep;225(3):303.e1-303.e17.

doi: 10.1016/j.ajog.2021.03.023. Epub 2021 Mar 26.

Coronavirus disease 2019 vaccine response in pregnant and lactating women: a cohort study

Kathryn J Gray¹, Evan A Bordt², Caroline Atyeo³, Elizabeth Deriso⁴, Babatunde Akinwunmi¹, Nicola Young⁵, Aranxta Medina Baez⁵, Lydia L Shook⁶, Dana Cvrk⁵, Kaitlyn James⁵, Rose De Guzman⁵, Sara Brigida⁵, Khady Diouf¹, Ilona Goldfarb⁵, Lisa M Bebell⁷, Lael M Yonker⁸, Alessio Fasano⁸, S Alireza Rabi⁹, Michal A Elovitz¹⁰, Galit Alter¹¹, Andrea G Edlow¹²

Affiliations

¹ Department of Obstetrics and Gynecology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA.
² Lurie Center for Autism, Department of Pediatrics, Massachusetts General Hospital, Harvard Medical School, Boston, MA.
³ Ragon Institute of MGH, MIT, and Harvard, Cambridge, MA; PhD Program in Virology, Division of Medical Sciences, Graduate School of Arts & Sciences, Harvard University, Boston, MA.
⁴ Ragon Institute of MGH, MIT, and Harvard, Cambridge, MA.
⁵ Department of Obstetrics and Gynecology, Massachusetts General Hospital, Harvard Medical School, Boston, MA.
⁶ Department of Obstetrics and Gynecology, Massachusetts General Hospital, Harvard Medical School, Boston, MA; Vincent Center for Reproductive Biology, Massachusetts General Hospital, Boston, MA.
⁷ Division of Infectious Diseases, Department of Medicine, Massachusetts General Hospital, Harvard Medical School, Boston, MA; MGH Center for Global Health, and Harvard Medical School, Boston, MA.
⁸ Mucosal Immunology and Biology Research Center, Massachusetts General Hospital, Boston, MA; Department of Pediatrics, Massachusetts General Hospital, Harvard Medical School, Boston, MA.
⁹ Department of Cardiothoracic Surgery, Massachusetts General Hospital, Harvard Medical School, Boston, MA.
¹⁰ Maternal and Child Health Research Center, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA.
¹¹ Ragon Institute of MGH, MIT, and Harvard, Cambridge, MA. Electronic address: galter@mgh.harvard.edu.
¹² Department of Obstetrics and Gynecology, Massachusetts General Hospital, Harvard Medical School, Boston, MA; Vincent Center for Reproductive Biology, Massachusetts General Hospital, Boston, MA. Electronic address: aedlow@mgh.harvard.edu.

PMID: 33775692
PMCID: PMC7997025
DOI: 10.1016/j.ajog.2021.03.023

Coronavirus disease 2019 vaccine response in pregnant and lactating women: a cohort study

Kathryn J Gray et al. Am J Obstet Gynecol. 2021 Sep.

. 2021 Sep;225(3):303.e1-303.e17.

doi: 10.1016/j.ajog.2021.03.023. Epub 2021 Mar 26.

Authors

Affiliations

¹ Department of Obstetrics and Gynecology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA.
² Lurie Center for Autism, Department of Pediatrics, Massachusetts General Hospital, Harvard Medical School, Boston, MA.
³ Ragon Institute of MGH, MIT, and Harvard, Cambridge, MA; PhD Program in Virology, Division of Medical Sciences, Graduate School of Arts & Sciences, Harvard University, Boston, MA.
⁴ Ragon Institute of MGH, MIT, and Harvard, Cambridge, MA.
⁵ Department of Obstetrics and Gynecology, Massachusetts General Hospital, Harvard Medical School, Boston, MA.
⁶ Department of Obstetrics and Gynecology, Massachusetts General Hospital, Harvard Medical School, Boston, MA; Vincent Center for Reproductive Biology, Massachusetts General Hospital, Boston, MA.
⁷ Division of Infectious Diseases, Department of Medicine, Massachusetts General Hospital, Harvard Medical School, Boston, MA; MGH Center for Global Health, and Harvard Medical School, Boston, MA.
⁸ Mucosal Immunology and Biology Research Center, Massachusetts General Hospital, Boston, MA; Department of Pediatrics, Massachusetts General Hospital, Harvard Medical School, Boston, MA.
⁹ Department of Cardiothoracic Surgery, Massachusetts General Hospital, Harvard Medical School, Boston, MA.
¹⁰ Maternal and Child Health Research Center, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA.
¹¹ Ragon Institute of MGH, MIT, and Harvard, Cambridge, MA. Electronic address: galter@mgh.harvard.edu.
¹² Department of Obstetrics and Gynecology, Massachusetts General Hospital, Harvard Medical School, Boston, MA; Vincent Center for Reproductive Biology, Massachusetts General Hospital, Boston, MA. Electronic address: aedlow@mgh.harvard.edu.

PMID: 33775692
PMCID: PMC7997025
DOI: 10.1016/j.ajog.2021.03.023

Abstract

Background: Pregnant and lactating women were excluded from initial coronavirus disease 2019 vaccine trials; thus, data to guide vaccine decision making are lacking.

Objective: This study aimed to evaluate the immunogenicity and reactogenicity of coronavirus disease 2019 messenger RNA vaccination in pregnant and lactating women compared with: (1) nonpregnant controls and (2) natural coronavirus disease 2019 infection in pregnancy.

Study design: A total of 131 reproductive-age vaccine recipients (84 pregnant, 31 lactating, and 16 nonpregnant women) were enrolled in a prospective cohort study at 2 academic medical centers. Titers of severe acute respiratory syndrome coronavirus 2 spike and receptor-binding domain immunoglobulin G, immunoglobulin A, and immunoglobulin M were quantified in participant sera (n=131) and breastmilk (n=31) at baseline, at the second vaccine dose, at 2 to 6 weeks after the second vaccine, and at delivery by Luminex. Umbilical cord sera (n=10) titers were assessed at delivery. Titers were compared with those of pregnant women 4 to 12 weeks from the natural infection (n=37) by enzyme-linked immunosorbent assay. A pseudovirus neutralization assay was used to quantify neutralizing antibody titers for the subset of women who delivered during the study period. Postvaccination symptoms were assessed via questionnaire. Kruskal-Wallis tests and a mixed-effects model, with correction for multiple comparisons, were used to assess differences among groups.

Results: Vaccine-induced antibody titers were equivalent in pregnant and lactating compared with nonpregnant women (pregnant, median, 5.59; interquartile range, 4.68-5.89; lactating, median, 5.74; interquartile range, 5.06-6.22; nonpregnant, median, 5.62; interquartile range, 4.77-5.98, P=.24). All titers were significantly higher than those induced by severe acute respiratory syndrome coronavirus 2 infection during pregnancy (P<.0001). Vaccine-generated antibodies were present in all umbilical cord blood and breastmilk samples. Neutralizing antibody titers were lower in umbilical cord than maternal sera, although this finding did not achieve statistical significance (maternal sera, median, 104.7; interquartile range, 61.2-188.2; cord sera, median, 52.3; interquartile range, 11.7-69.6; P=.05). The second vaccine dose (boost dose) increased severe acute respiratory syndrome coronavirus 2-specific immunoglobulin G, but not immunoglobulin A, in maternal blood and breastmilk. No differences were noted in reactogenicity across the groups.

Conclusion: Coronavirus disease 2019 messenger RNA vaccines generated robust humoral immunity in pregnant and lactating women, with immunogenicity and reactogenicity similar to that observed in nonpregnant women. Vaccine-induced immune responses were statistically significantly greater than the response to natural infection. Immune transfer to neonates occurred via placenta and breastmilk.

Keywords: COVID-19 vaccine; antibodies; breastfeeding; breastmilk; cord blood; mRNA; maternal immunity; neonatal immunity; pregnancy.

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Figures

**Figure 1**
Maternal vaccination induces a robust SARS-CoV-2–specific antibody response **A–D,** Violin plots show the log₁₀ transformed mean fluorescence intensity (MFI) for (A) IgG spike-, (B) IgG RBD-, (C) IgA spike-, and (D) IgA RBD–specific titers across V0, V1, and V2 time points collected from nonpregnant of reproductive age (blue), pregnant (orange), or lactating (purple) participants. Participants who received BNT 162b2 from Pfizer/BioNTech are depicted as *open circles*, and participants who received mRNA-1273 from Moderna/NIH are depicted as *closed circles*. Differences across time points and groups were assessed by repeated measures mixed-effects model followed by post hoc Tukey’s multiple comparisons test. The *asterisk* indicates P<.05, the *double asterisk* indicates P<.01, the *triple asterisk* indicates P<.001, and the *quadruple asterisk* indicates P<.0001. E, Line graph showing the log₁₀ transformed relative spike-specific titers across V0, V1, and V2 time points collected from nonpregnant (blue), pregnant (orange), or lactating (purple) participants for IgG (*circles and solid lines*), IgM (*open triangles and dashed lines*), and IgA (*squares and dotted lines*). F, Violin plots show the IgG and IgM spike–specific titer in nonpregnant (blue), pregnant (orange), lactating (purple), and naturally-infected pregnant (yellow) participants. Participants who received BNT 162b2 from Pfizer/BioNTech are depicted as *open circles*, and participants who received mRNA-1273 from Moderna/NIH are depicted as *closed circles*. Differences across groups were assessed by Kruskal-Wallis test followed by post hoc Dunn’s multiple comparisons test. The *quadruple asterisk* indicates P<.0001 compared with natural infection in pregnant women. Ig, immunoglobulin; *mRNA*, messenger RNA; *RBD*, receptor-binding domain; *SARS-CoV-2*, severe acute respiratory syndrome coronavirus 2. *Gray et al. Coronavirus disease 2019 vaccination in pregnancy and lactation. Am J Obstet Gynecol 2021.*

**Figure 2**
Placental and breastmilk transfer of vaccine-induced SARS-CoV-2 antibodies **A–C,** Violin plots show the log₁₀ transformed mean fluorescence intensity (MFI) for (A) IgG1-, (B) IgA-, and (C) IgM spike–specific breastmilk titers across V0, V1, and V2 time points. Differences across time points were assessed with repeated measures mixed-effects model followed by post hoc Tukey’s multiple comparisons test. Participants who received BNT 162b2 from Pfizer/BioNTech are depicted as *open circles*, and participants who received mRNA-1273 from Moderna/NIH are depicted as *closed circles*. The *asterisk* indicates P<.05, the *double asterisk* indicates P<.01, the *triple asterisk* indicates P<.001, and the *quadruple asterisk* indicates P<.0001. **D–E,** Dot plots showing relative (D) spike- and (E) RBD-specific maternal blood (M) and cord blood (C) titers of IgG1. Wilcoxon matched-pairs signed rank test was performed to determine significance. At the right of each panel, the x-axis shows the time from the second vaccine to delivery and the y-axis shows cord blood log₁₀ transformed titer for (D) IgG spike (purple) and (E) IgG RBD (turquoise). Correlation was determined by Spearman correlation test. PBS background subtraction was used to determine corrected optical density (OD) of 0.0. F, Neutralizing antibody titers (50% inhibitory dose) of maternal blood (M) and cord blood (C) are presented. Wilcoxon matched-pairs signed rank test was performed to determine significance. Ig, immunoglobulin; *PBS*, phosphate-buffer saline; *RBD*, receptor-binding domain; *SARS-CoV-2*, severe acute respiratory syndrome coronavirus 2; TR, transfer ratio. *Gray et al. Coronavirus disease 2019 vaccination in pregnancy and lactation. Am J Obstet Gynecol 2021.*

**Supplemental Figure 1**
Maternal vaccination induces robust SARS-CoV-2–specific antibodies in maternal serum **A–B,** Violin plots show the log₁₀ transformed mean fluorescence intensity (MFI) for (A) IgM spike– and (B) IgM RBD–specific titers across V0, V1, and V2 time points collected from nonpregnant controls (blue), pregnant (orange), or lactating (purple) patients. Participants injected with BNT 162b2 from Pfizer/BioNTech are depicted as *open circles*, and participants injected with mRNA-1273 from Moderna/NIH are depicted as *closed circles*. Differences across time points and groups were assessed by repeated measures mixed-effects model followed by post hoc Tukey’s multiple comparisons test. The *asterisk* indicates P<.05, the *double asterisk* indicates P<.01, the *triple asterisk* indicates P<.001, and the *quadruple asterisk* indicates P<.0001. The *dotted line* depicts PBS background level. C, Line graph showing the log₁₀ transformed relative spike-specific titers across V0, V1, and V2 time points collected from nonpregnant controls (blue), pregnant (orange), or lactating (purple) patients for IgG (*circles and solid lines*) and IgA (*squares and dotted lines*). The *dotted line* depicts PBS background level. **D–I,** Violin plots show the log₁₀ transformed (D) IgM S1–, (E) IgM S2–, (F) IgG S1–, (G), IgG S2–, (H) IgA S1–, and (I) IgA S2–specific titers across V0, V1, and V2 time points collected from nonpregnant controls (blue), pregnant (orange), or lactating (purple) patients. Participants injected with BNT 162b2 from Pfizer/BioNTech are depicted as *open circles*, and participants injected with mRNA-1273 from Moderna/NIH are depicted as *closed circles*. Differences across time points and groups were assessed by repeated measures mixed-effects model followed by post hoc Tukey’s multiple comparisons test. The *asterisk* indicates P<.05, the *double asterisk* indicates P<.01, the *triple asterisk* indicates P<.001, the *quadruple asterisk* indicates P<.0001. Ig, immunoglobulin; *NIH*, National Institutes of Health; *PBS*, phosphate-buffer saline; *SARS-CoV-2*, severe acute respiratory syndrome coronavirus. *Gray et al. Coronavirus disease 2019 vaccination in pregnancy and lactation. Am J Obstet Gynecol 2021.*

**Supplemental Figure 2**
mRNA-1273 (Moderna/NIH) induces a greater IgA response than does BNT 162b2 (Pfizer/BioNTech) **A–C,** Violin plots show the log₁₀ transformed mean fluorescence intensity (MFI) for (A) IgA spike–, (B) IgG spike–, and (C) IgM spike–specific titers across V1 and V2 time points collected from nonpregnant (blue), pregnant (orange), or lactating (purple) participants receiving either mRNA-1273 (Moderna) or BNT 162b2 (Pfizer). Differences across time points and groups were assessed by repeated measures mixed-effects model followed by post hoc Tukey’s multiple comparisons test. The *dotted line* depicts PBS background level. The *asterisk* indicates P<.05, the *double asterisk* indicates P<.01, the *triple asterisk* indicates P<.001, the *quadruple asterisk* indicates P<.0001. Ig, immunoglobulin; *mRNA*, messenger RNA; *NIH*, National Institutes of Health; *PBS*, phosphate-buffer saline. *Gray et al. Coronavirus disease 2019 vaccination in pregnancy and lactation. Am J Obstet Gynecol 2021.*

**Supplemental Figure 3**
Neither trimester of infection nor vaccination affect SARS-CoV-2 antibody production A, Violin plots show the IgG spike–specific titer induced by vaccination during the first trimester (red), second trimester (orange), or third trimester (yellow). Participants who received BNT 162b2 from Pfizer/BioNTech are depicted as *open circles*, and participants who received mRNA-1273 from Moderna/NIH are depicted as *closed circles*. Differences across groups were assessed by Kruskal-Wallis test. Kruskal-Wallis P=.48. B, Violin plots show the IgG spike–specific of naturally-infected pregnant women infected during the second trimester (yellow) or third trimester (brown). Differences across groups were assessed by Mann-Whitney test. Mann-Whitney P=.48. Ig, immunoglobulin; *mRNA*, messenger RNA; OD, optical density; *SARS-CoV-2*, severe acute respiratory syndrome coronavirus 2. *Gray et al. Coronavirus disease 2019 vaccination in pregnancy and lactation. Am J Obstet Gynecol 2021.*

**Supplemental Figure 4**
Maternal vaccination induces SARS-CoV-2–specific antibodies in breastmilk **A–I,** Violin plots show the log₁₀ transformed mean fluorescence intensity (MFI) for (A) IgG1 RBD–, (B) IgA RBD–, (C) IgM RBD, (D) IgG1 S1–, (E) IgA S1–, and (F) IgM S1–, (G) IgG1 S2–, (H) IgA S2–, and (I) IgM S2–specific breastmilk titers across V0, V1, and V2 time points. Differences across time points were assessed with repeated measures mixed-effects model followed by post hoc Tukey’s multiple comparisons test. Participants injected with BNT 162b2 from Pfizer/BioNTech are depicted as *open circles*, and participants injected with mRNA-1273 from Moderna/NIH are depicted as *closed circles*. The *dotted line* depicts PBS background level. The *asterisk* indicates P<.05, the *double asterisk* indicates P<.01, the *triple asterisk* indicates P<.001, and the *quadruple asterisk* indicates P<.0001. Ig, immunoglobulin; *PBS*, phosphate-buffer saline; *RBD*, receptor-binding domain; *SARS-CoV-2*, severe acute respiratory syndrome coronavirus 2. *Gray et al. Coronavirus disease 2019 vaccination in pregnancy and lactation. Am J Obstet Gynecol 2021.*

**Supplemental Figure 5**
Transfer of SARS-CoV-2–specific antibodies from maternal to umbilical cord blood following maternal vaccination **A–B,** The x-axis shows the time from V2 until delivery and the y-axis shows cord blood log₁₀ transformed titer for (A) IgG3 spike (purple) and (B) IgG3 RBD (turquoise). Significance and rho were determined by Spearman’s correlation test. Ig, immunoglobulin; *MFI*, mean fluorescence intensity; *SARS-CoV-2*, severe acute respiratory syndrome coronavirus 2. *Gray et al. Coronavirus disease 2019 vaccination in pregnancy and lactation. Am J Obstet Gynecol 2021.*

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Update of

COVID-19 vaccine response in pregnant and lactating women: a cohort study.
Gray KJ, Bordt EA, Atyeo C, Deriso E, Akinwunmi B, Young N, Baez AM, Shook LL, Cvrk D, James K, De Guzman RM, Brigida S, Diouf K, Goldfarb I, Bebell LM, Yonker LM, Fasano A, Rabi SA, Elovitz MA, Alter G, Edlow AG. Gray KJ, et al. medRxiv [Preprint]. 2021 Mar 8:2021.03.07.21253094. doi: 10.1101/2021.03.07.21253094. medRxiv. 2021. Update in: Am J Obstet Gynecol. 2021 Sep;225(3):303.e1-303.e17. doi: 10.1016/j.ajog.2021.03.023 PMID: 33758889 Free PMC article. Updated. Preprint.

Comment in

Accommodating vaccine preferences among women of childbearing age.
Czeisler MÉ, Rajaratnam SMW, Howard ME, Czeisler CA. Czeisler MÉ, et al. Am J Obstet Gynecol. 2021 Dec;225(6):697-699. doi: 10.1016/j.ajog.2021.07.017. Epub 2021 Jul 31. Am J Obstet Gynecol. 2021. PMID: 34343503 Free PMC article. No abstract available.

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References

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[1] CDC COVID-19 Response Team; Food and Drug Administration Allergic reactions including anaphylaxis after receipt of the first dose of Moderna COVID-19 vaccine—United States, December 21, 2020-January 10, 2021. MMWR Morb Mortal Wkly Rep. 2021;70:125–129. - PMC - PubMed

[2] CDC COVID-19 Response Team; Food and Drug Administration Allergic reactions including anaphylaxis after receipt of the first dose of Moderna COVID-19 vaccine—United States, December 21, 2020-January 10, 2021. MMWR Morb Mortal Wkly Rep. 2021;70:125–129. - PMC - PubMed

[3] Zambrano L.D., Ellington S., Strid P., et al. Update: characteristics of symptomatic women of reproductive age with laboratory-confirmed SARS-CoV-2 infection by pregnancy status - United States, January 22-October 3, 2020. MMWR Morb Mortal Wkly Rep. 2020;69:1641–1647. - PMC - PubMed

[4] Zambrano L.D., Ellington S., Strid P., et al. Update: characteristics of symptomatic women of reproductive age with laboratory-confirmed SARS-CoV-2 infection by pregnancy status - United States, January 22-October 3, 2020. MMWR Morb Mortal Wkly Rep. 2020;69:1641–1647. - PMC - PubMed

[5] Krammer F. SARS-CoV-2 vaccines in development. Nature. 2020;586:516–527. - PubMed

[6] Krammer F. SARS-CoV-2 vaccines in development. Nature. 2020;586:516–527. - PubMed

[7] Creech C.B., Walker S.C., Samuels R.J. SARS-CoV-2 vaccines. JAMA. 2021 [Epub ahead of print] - PubMed

[8] Creech C.B., Walker S.C., Samuels R.J. SARS-CoV-2 vaccines. JAMA. 2021 [Epub ahead of print] - PubMed

[9] Bianchi D.W., Kaeser L., Cernich A.N. Involving pregnant individuals in clinical research on COVID-19 vaccines. JAMA. 2021;325:1041–1042. - PMC - PubMed

[10] Bianchi D.W., Kaeser L., Cernich A.N. Involving pregnant individuals in clinical research on COVID-19 vaccines. JAMA. 2021;325:1041–1042. - PMC - PubMed

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Coronavirus disease 2019 vaccine response in pregnant and lactating women: a cohort study

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Coronavirus disease 2019 vaccine response in pregnant and lactating women: a cohort study

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