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Maternal and Neonatal Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) Immunoglobulin G Levels After the Pfizer-BioNTech Booster Dose for Coronavirus Disease 2019 (COVID-19) Vaccination During the Second Trimester of Pregnancy

Kugelman, Nir MD; Nahshon, Chen MD; Shaked-Mishan, Pninit PhD; Kleifeld, Shiran MD; Cohen, Nadav MD; Sher, Maayan Lahav MD; Zahran, Hazar MD; Barsha, Hanin MD; Assaf, Wisam MD; Shalabna, Eiman MD; Stein, Nili MPH; Lavie, Ofer MD; Kedar, Reuven MD; Riskin-Mashiah, Shlomit MD

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Obstetrics & Gynecology: May 27, 2022 - Volume - Issue - 10.1097/AOG.0000000000004867
doi: 10.1097/AOG.0000000000004867
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The Pfizer-BioNTech messenger RNA (Pfizer) coronavirus disease 2019 (COVID-19) vaccine was found to be highly effective in preventing symptomatic and severe COVID-19 in pregnant women.1,2 However, protection from the vaccine reduces with time.3 The administration of a third COVID-19 dose (booster dose) has been authorized and recommended to pregnant women by several health organizations to reestablish protection.4,5 It has been demonstrated that a third dose of the Pfizer COVID-19 vaccine is effective in restoring protection against severe COVID-19–related outcomes and decreases rates of hospitalizations compared with those who received only two doses at least 5 months before.6–8

Previous studies have demonstrated a robust maternal antibody response and placental transmission of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) antibodies after COVID-19 vaccination during the second and third trimesters.1,2,9–13 Recent studies also show that SARS-CoV-2 antibody titers 1 month after administration of the Pfizer COVID-19 vaccine were higher among nonpregnant participants who received a third vaccine dose compared with those who received the second vaccine dose.14,15 Additionally, it has been found that higher antibody titers correlate with higher vaccine efficacy.16

There are limited data regarding the immunologic response in pregnant women after administration of the third Pfizer COVID-19 vaccine during pregnancy. In this study, we evaluated maternal and neonatal SARS-CoV-2 immunoglobulin G (IgG) antibody levels at birth after administration of the third (booster) dose of Pfizer COVID-19 vaccine during the second trimester of pregnancy. We also compared these antibody levels with those in a previously published control group of pregnant women who received only two Pfizer COVID-19 vaccine doses during the same gestational age window.

METHODS

This was a prospective cohort study, conducted between October 2021 and February 2022 at the delivery ward of Carmel Medical Center, Haifa, Israel. The study was approved by the Carmel Medical Center Institutional Review Board on August 24, 2021 (protocol number CMC-0051-21).

Pregnant women at more than 24 weeks of gestation with singleton pregnancies who were expected to give birth within 3 days and who had received the third dose of Pfizer COVID-19 vaccine (booster group) at 17–30 weeks of pregnancy and were not known to have a previous infection with the virus (negative results in all previous SARS-CoV-2 tests that were performed, for example, because of symptoms, exposure to people with infection, for isolation reduction, before travel) were enrolled and recruited consecutively on admission to the delivery ward. All women had received the third Pfizer COVID-19 vaccine at least 5 months after their second Pfizer COVID-19 vaccination, and none were immunocompromised. Written informed consent was obtained from all study participants before enrollment.

A maternal blood sample was obtained after enrollment, and an umbilical cord blood sample was obtained within 30 minutes after birth. Both maternal and umbilical cord blood samples were assessed using SARS-CoV-2 IgG II Quant [email protected], a two-step chemiluminescent microparticle immunoassay used for the quantitative determination of IgG antibodies to SARS-CoV-2 on Architect and Alinity i systems. The SARS-CoV-2 IgG II Quant assay is designed to detect IgG antibodies, including neutralizing antibodies, to the receptor-binding domain of the S1 subunit of the spike protein of SARS-CoV-2 virus in human serum and plasma.

At the time of recruitment, demographic and clinical data were collected, including maternal age; body mass index (BMI, calculated as weight in kilograms divided by height in meters squared); self-reported ethnicity; history of systemic disease and chronic medications; parity; date and gestational age at the first, second, and third vaccines; systemic side effects after each vaccine; and gestational age at birth. The time interval between the third vaccine and birth was calculated. Further data were abstracted from patients' medical records after birth, including stillbirth, mode of birth, neonatal sex, neonatal weight, 5-minute Apgar score, and neonatal intensive care unit admission. The correlation between antibody titers, fetal–maternal characteristics, and the time interval from the last vaccination to birth were analyzed. In addition, transplacental SARS-CoV-2 IgG antibody transfer ratios were calculated by dividing neonatal (umbilical cord blood) IgG levels by the IgG antibody levels in paired maternal blood. Subsequently, correlation between transplacental SARS-CoV-2 IgG antibody transfer ratios and gestational age at the third COVID-19 vaccination was analyzed.

A secondary analysis was performed to compare the booster group with a historical control group who received the second Pfizer COVID-19 vaccine dose (two-dose group) at 17–30 weeks of gestation. The control (two-vaccine) group was from a previously published study conducted by our group at the same medical center between May 2021 and July 2021, evaluating maternal and neonatal antibody SARS-CoV-2 antibody levels at birth after receipt of two COVID-19 vaccine doses during the second trimester.13 The correlation between maternal and neonatal SARS-CoV-2 IgG antibody levels and the duration from the last vaccine dose at a time interval of 10–20 weeks from the second or third COVID-19 vaccination was analyzed and compared between the groups. This time interval was chosen for comparison because most of the available data for both groups were from within this time frame.

Continuous variables are presented as means and SDs or as medians and interquartile ranges. Categorical variables are presented as percentages. Characteristics of the booster group were compared with those of the two-dose group using χ2 for the categorical variables and independent t test or Mann-Whitney, as appropriate, for the continuous variables. To estimate correlations with antibody levels, we used a univariable linear model (maternal and neonatal separately) with a logarithmic transformation for the antibody level because it is not normally distributed. Variables that were found to be statistically significant (two-sided P<.05) were entered into a stepwise multivariable linear regression model to estimate adjusted associations with antibody levels. Correlations between the maternal and neonatal antibody levels, between transplacental antibody transfer ratio and gestational age at the third COVID-19 vaccination, and between antibody levels and duration from last vaccine to birth were analyzed using the Spearman correlation. Prediction intervals were calculated for the regression line demonstrating the correlation between neonatal and maternal antibody levels after the third vaccination. The 95% CI for the correlation coefficient was performed using SAS 9.4. All other analyses were performed using IBM SPSS Statistics 24.

RESULTS

Between October 2021 and February 2022, 121 women were enrolled in the booster group. Umbilical cord blood was collected from 109 neonates. Of 12 neonates whose antibody titers were not measured, 11 did not have samples obtained and one sample was not analyzed due to insufficient blood volume. Demographic and clinical characteristics are presented in Table 1. Mean±SD gestational age at birth was 39.1±1.5 weeks, an average of 15.3±3.9 weeks after the third vaccine. All maternal and neonatal SARS-CoV-2 IgG test results were positive. Median (interquartile range) level of IgG antibodies at birth was 4,485.3 (2,569.0–9,702.7) AU/mL for women and 8,773.3 (5,143.8–18,830.9) AU/mL for neonates. There was a strong positive correlation between neonatal SARS-CoV-2 IgG antibody titers at birth and maternal antibody titers (slope=0.9, 95% CI 0.83–0.96, P<.001); prediction line mean (lower limit, upper limit): 9,701 (5,586, 17,154) AU/mL (Fig. 1). For each 1% increase in maternal antibody level, neonatal antibody levels increased by 1.0% (95% CI 0.9–1.1, P<.001). Neonatal titers measured, on average, two times higher than maternal titers, with a mean±SD transplacental SARS-CoV-2 IgG antibody transfer ratio of 2.1±0.5. No correlation between transplacental SARS-CoV-2 IgG antibody transfer ratio and gestational age at the third COVID-19 vaccination was found (r=−0.04, 95% CI −0.22 to 0.14, P=.657) (Fig. 2).

Table 1. - Characteristics of Pregnant Women Who Received the Third (Booster) Dose Compared With the Primary Two-Dose Vaccination Series of Pfizer-BioNTech Messenger RNA Coronavirus Disease 2019 (COVID-19) Vaccine During the Second Trimester of Pregnancy
Characteristic Booster Group Two-Dose Group P
Maternal n=121 n=121
 Age (y) 32.5±4.2 32.1±4.8 .426
 BMI (kg/m2) 28.6±4.6 27.9±5.4 .301
 Underlying medical comorbidities* 29 (24.0) 25 (20.7) .537
 Primiparous 42 (34.7) 56 (46.3) .067
 Systemic side effects after vaccine
  1st dose 12 (9.9) 14 (11.6) .843
  2nd dose 30 (24.8) 39 (32.2) .260
  3rd dose 24 (19.8)
  Any dose 44 (36.4) 44 (36.4) .999
 Gestational age (wk)
  At receipt of last vaccine dose 23.8±3.6 24.5±2.8 .083
  At birth 39.1±1.5 39.2±1.4 .872
 Time interval from last vaccine dose to birth (wk) 15.3±3.9 14.6±2.6 .103
Neonatal n=109 n=107
 Male sex 55 (50.4) 59 (55.1) .583
 Birth weight (g) 3,226.3±480.3 3,256.3±422.6 .627
BMI, body mass index.
Data are mean±SD or n (%) unless otherwise specified.
*Primary two-dose vaccination group: diabetes (seven women), hypertensive disease (five women), thyroid disease (five women), asthma (four women), Crohn's disease (one woman), multiple sclerosis (one woman), celiac disease (one woman), familial Mediterranean fever (one woman); booster group: diabetes (11 women), hypertensive disease (five women), thyroid disease (10 women), asthma (three women).
General weakness, dizziness, fever, chills, headache, vomiting, general muscle aches, fatigue, general rash.

F1
Fig. 1.:
Correlation between maternal severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) immunoglobulin G (IgG) antibodies and neonatal SARS-CoV-2 IgG antibodies after the third coronavirus 2019 (COVID-19) vaccination. Slope: 0.9, 95% CI 0.83–0.96, P<.001; prediction line mean (lower limit, upper limit): 9,701 (5,586, 17,154) AU/mL. Dashed lines indicate upper and lower limits. Solid line indicates prediction line.
F2
Fig. 2.:
Correlation between transplacental severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) immunoglobulin G (IgG) antibody transfer ratio and gestational age at the third coronavirus 2019 vaccination. R=−0.04, 95% CI ‒0.22 to 0.14, P=.657.

The booster group was compared with the two-dose group, which included 121 women and 107 neonates, with SARS-CoV-2 IgG levels measured at a mean±SD of 14.6±2.6 weeks after the second vaccine. No significant differences were found between groups for demographic or clinical characteristics (Table 1). Maternal and neonatal outcomes were also similar between the groups (Table 2). Median [interquartile range] maternal SARS-CoV-2 IgG antibody titers were significantly higher in the booster group (4,485 [2,569–9,702] AU/mL) compared with the two-dose group (1,122 [735–1,872] AU/mL) (P<.001). Furthermore, neonatal SARS-CoV-2 IgG antibody titers were significantly higher in the booster group (8,773 [5,143–18,830] AU/mL) compared with the two-dose group (3,280 [2,087–5,754] AU/mL) (P<.001). The comparison of SARS-CoV-2 IgG antibody levels between the groups is presented in Figures 3 and 4.

Table 2. - Maternal and Neonatal Third (Booster) Dose Compared With Primary Two-Dose Vaccination Series of Pfizer-BioNTech Messenger RNA Coronavirus Disease 2019 (COVID-19) Vaccine During the Second Trimester of Pregnancy
Outcome Booster Group (n=121) Two-Dose Group (n=121) P
Mode of birth
 Spontaneous vaginal 85 (70.2) 94 (77.7) .237
 Vacuum-assisted 4 (3.3) 1 (0.8)
 Cesarean 32 (26.5) 26 (21.5)
Preterm birth (less than 37 wk) 9 (7.4) 9 (7.4) .808
Stillbirth 0 (0) 0 (0) >.99
Birth weight (g)
 2,500 or less 8 (6.6) 4 (3.3) .377
 4,000 or more 4 (3.3) 6 (4.9) .752
5-min Apgar score 7 or lower 1 (0.8) 0 (0) >.99
NICU admission 4 (3.3) 5 (4.1) >.99
NICU, neonatal intensive care unit.
Data are n (%) unless otherwise specified.

F3
Fig. 3.:
Correlation between maternal severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) immunoglobulin G antibodies and the duration from the last vaccine at a time interval of 10–20 weeks from the second or third coronavirus 2019 (COVID-19) vaccination. Second vaccine: slope=−0.24, 95% CI ‒0.18 to −0.09, P<.001; third vaccine: slope=−0.07, 95% CI ‒0.13 to −0.01, P=.019; slope difference: 0.07, 95% CI 0.02–0.14, P=.045.
F4
Fig. 4.:
Correlation between neonatal severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) immunoglobulin G antibodies and the duration from the last vaccine at a time interval of 10–20 weeks from the second or third coronavirus 2019 (COVID-19) vaccination. Second vaccine: slope=−0.14, 95% CI ‒0.19 to −0.08, P<.001; third vaccine: slope=−0.09, 95% CI ‒0.15 to −0.03, P=.004; slope difference: 0.05, 95% CI ‒0.03 to 0.13, P=.238.

There was a negative correlation between the time interval from vaccination and maternal SARS-CoV-2 IgG antibody levels when examining the time interval of 10–20 weeks from the second or third COVID-19 vaccination (Fig. 3) (second vaccine: slope=−0.24, 95% CI −0.18 to −0.09, P<.001; third vaccine: slope=−0.07, 95% CI −0.13 to −0.01, P=.019). The decline in maternal SARS-CoV-2 IgG antibody levels was slower in the booster group compared with the two-dose group (slope difference: 0.07, 95% CI 0.02–0.14, P=.045). The negative correlation between the time interval of 10–20 weeks from the second or third COVID-19 vaccination and neonatal SARS-CoV-2 IgG antibody levels is shown in Figure 4 (second vaccine: slope=−0.14, 95% CI −0.19 to −0.08, P<.001; third vaccine: slope=−0.09, 95% CI −0.15 to −0.03, P=.004). The decline in neonatal SARS-CoV-2 IgG antibody levels was similar in the booster group compared with the two-dose group (slope difference: 0.05, 95% CI −0.03 to 0.13, P=.238).

Multivariable analysis revealed an inverse correlation between maternal titers during the delivery admission and the time interval from the third vaccination. In the range of 5–23 weeks elapsed since the receipt of the third vaccine dose, for each week that passed, maternal antibody levels dropped by −6.5% (95% CI −9.8% to −3.0%, P=.001).

In multivariable analysis, maternal antibody titers and maternal age remained significantly correlated with neonatal antibody titers. For each 1% increase in maternal antibody level, neonatal antibody levels increased by 0.9% (95% 0.8–1.0, P<.001). Furthermore, for each 1-year increase in maternal age, neonatal antibody levels decreased by −1.8% (95% CI −3.1% to −0.5%, P=.008).

DISCUSSION

This prospective study demonstrated significantly higher maternal and neonatal SARS-CoV-2 IgG antibody levels at birth after a second-trimester booster (third dose) of maternal Pfizer COVID-19 vaccination compared with the primary two-dose vaccination series. Beginning 5 weeks after receipt of the last vaccine, both maternal and neonatal antibody titers decreased with a longer time interval between vaccine administration and time of birth. However, the decline in maternal antibodies was slower in the booster group.

Placental transmission of SARS-CoV-2 antibodies has previously been proven in multiple studies.1,2,9–13 In the general (nonpregnant) population, the booster vaccination dose has been shown to yield a better immune response and protection compared with the two-dose vaccination series.14,16,17 Our study supplements existing work by analyzing the association between booster vaccination and antibody levels in pregnant women and their neonates.

A previous study by Yang et al18 showed that maternal and neonatal IgG titers were higher in women receiving a booster vaccination dose compared with women receiving the primary two-dose series; however, they included only 18 women receiving a booster vaccination dose.

Maternal vaccination is recommended throughout pregnancy to minimize the risk of severe COVID-19 for both the mother and her fetus.1 The goal of maternal COVID-19 vaccination is to provide maximal maternal and neonatal protection during pregnancy and after birth; thus, understanding the immune response is important. According to the present and numerous previous studies, antibody titers decrease with time—thus the recommendation for a booster (third) vaccine dose 5 months after the primary two-dose vaccination series. In our study, all mothers and neonates had positive SARS-CoV-2 IgG results after second-trimester vaccination. Furthermore, maternal and neonatal SARS-CoV-2 IgG antibody levels at birth were significantly higher in the booster group compared with the two-dose group, demonstrating the importance of the booster dose in eligible pregnant women. Also, the rate of decline in maternal antibody levels was slower in the booster group compared with the two-dose group. These results suggest that a booster vaccination during pregnancy may provide better and longer COVID-19 protection for pregnant women. Higher titers in cord blood after a maternal booster dose may also result in longer and better protection for neonates, but this observed association needs further study.

Our study has several strengths. This is a prospective study comparing two large groups with similar demographic and clinical characteristics, supporting our conclusion that the higher antibody level is due to an additional vaccination dose. Furthermore, all women received the same vaccine, and none had a known previous diagnosis of SARS-CoV-2 infection.

The study also has several limitations. This is a single-center study with an ethnically homogeneous population, and all women received the Pfizer COVID-19 vaccine; thus, the results might not be applicable to other vaccines or settings. We assumed that women did not have infection based on previous tests; however, some women may have had asymptomatic or mild illness without confirmed diagnosis. Our laboratory uses an antibody test that also recognizes IgG to nucleocapsid protein; thus, an occult natural infection may have led to an increased immune response in some women. However, during the period of the Omicron variant, SARS-CoV-2 tests (PCR or antigen) were very accessible to the public in Israel and were even provided by the government. People were tested not only due to symptoms but also after exposure to people with infection, for isolation reduction, and before travel, so the risk of undetected infection is mitigated compared with populations without test availability; the majority of women included in this study had several SARS-CoV-2 tests in the months prior their deliveries. Another limitation of our study is that maternal SARS-CoV-2 IgG antibodies were not evaluated before the third vaccination. Therefore, it is possible that the results may reflect higher antibody levels preceding the third dose, resulting in higher postvaccination antibodies compared with the two-dose group.

Maternal and neonatal SARS-CoV-2 IgG antibody titers after second-trimester maternal Pfizer COVID-19 vaccination were significantly higher after the third (booster) dose compared with the primary two-dose vaccination series. Although there is uncertainty as to whether antibody levels correlate with protection, these data help support the importance of messenger RNA COVID-19 booster vaccination during pregnancy to restore and enhance maternal and neonatal protection against COVID-19.

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