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. 2023 Jan 6;156:103798. doi: 10.1016/j.jri.2023.103798

Vaccination options for pregnant women during the Omicron period

Jiarui He 1,1, Zichun Wei 1,1, Taiyang Leng 1, Jiaqi Bao 1, Xinyao Gao 1, Fei Chen 1,⁎
PMCID: PMC9817340  PMID: 36640675

Abstract

Omicron exhibits reduced pathogenicity in general population than the previous severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) variants. However, the severity of disease and pregnancy outcomes of Omicron infection among pregnant women have not yet been definitively established. Meanwhile, substantial proportions of this population have doubts about the necessity of vaccination given the reports of declining efficacy of coronavirus disease 2019 (COVID-19) vaccines. Herein, we comprehensively discuss the clinical outcomes of infected pregnant women during the Omicron period and summarize the available data on the safety and efficacy profile of COVID-19 vaccination. The results found that the incidence of moderate and severe disease, maternal mortality, pregnancy loss, preterm delivery, stillbirth, preeclampsia/eclampsia, and gestational hypertension during the Omicron period are similar to those during the Pre-Delta period. In view of the effects of mass vaccination and previous natural infection on disease severity, the virulence of Omicron in pregnant women may be comparable to or even higher than that of the Pre-Delta variant. Moreover, the currently approved COVID-19 vaccines are safe and effective for pregnant women. Particularly, those who received a second or third dose had significantly less severe disease with little progression to critical illness or death compared with those who were unvaccinated or received only one dose. Therefore, in the case of the rapid spread of Omicron, pregnant women should still strictly follow preventive measures to avoid infection and receive the COVID-19 vaccine in a timely manner.

Keywords: COVID-19, Omicron, Maternal mortality, Pregnancy outcomes, Vaccination

1. Introduction

The continuous evolution of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has led to the emergence of multiple variants. To prioritize global monitoring and research of these variants, the World Health Organization (WHO) classified them into three categories: variants of interest, variants under monitoring and variants of concern (VOCs). The previous four VOCs include Alpha (B.1.1.7), Beta (B.1.351), Gamma (P.1) and Delta (B.1.617.2) (World Health Organization, 2022b). All of them have higher transmissibility and immune evasion potential than early wild-type strain and lead to a new wave of pandemic and thousands of deaths across the whole world (Tian et al., 2021). In November 2021, a new variant named Omicron (B. 1.1. 529) was designated as the fifth VOC by WHO, which immediately attracted much attention from the general public. Initial analysis of the genetic sequence of Omicron revealed more than 60 mutations in the genome, making it the most highly mutated VOC to date (CoVariants, 2022). Particularly, it harbors 37 amino acid substitutions in the spike protein, 15 of them are in the receptor-binding domain (RBD) (Centers for Disease Control and Prevention, 2021). N501Y, Q498R, Q493R, S375F, S373P, S371L and T478K mutations can significantly enhance the binding of the RBD to angiotensin-converting enzyme 2 (ACE2), enabling Omicron to be more transmissible (Kumar et al., 2022). H655Y, N679K and P681H mutations are present near the furin cleavage site and linked with enhanced replication ability and infectivity (Centers for Disease Control and Prevention, 2021). Therefore, it is not difficult to understand that Omicron has rapidly replaced Delta as the most predominant form of SARS-CoV-2 circulating globally.

The mutations in the non-RBD regions altered cell tropism of the virus (Fan et al., 2022). Specifically, Omicron replicated poorly in Calu-3 cells with high expression of transmembrane serine protease 2, exhibiting a weaker cell-cell fusion activity. However, it replicated well in cells that support endosomal entry (Zhao et al., 2022, Willett et al., 2022). It is important because this restricts the virus to the upper respiratory tract and makes it less likely to spread in the lungs. This contention is supported by studies in human ACE2-expressing mice and Syrian hamsters, which found that Omicron infection causes milder lung pathology (Bentley et al., 2021, Mcmahan et al., 2022). Thus, Omicron has a less severe clinical presentation in the general population compared to the previous VOCs. According to a recent report, the proportion of asymptomatic infections for Omicron is as high as 80–90% (Murray, 2022). The rate of hospitalization, intensive care unit (ICU) admission, and receipt of invasive mechanical ventilation among persons aged ≥ 50 years were lower during the Omicron-predominant period than during the Delta-predominant period, and the median length of hospital stay was also considerably shorter (Iuliano, 2022). Additionally, the death toll from Omicron in most countries is nearly identical to that of a severe influenza season in northern hemisphere countries (Murray, 2022). However, these data on the clinical outcomes of Omicron infection have been derived mostly from countries with high vaccination rates.

Pregnant women are thought to be more susceptible to COVID-19 than the general population given the physiological adaptive changes and immunosuppressive state during pregnancy. Notably, infection with wild-type SARS-CoV-2 is associated with an increased risk of cesarean delivery and pregnancy complications (Li et al., 2020). Given the lower pathogenicity of the Omicron, some people suggested that the clinical manifestations and outcomes of pregnant women infected with this variant are milder than those of previous VOCs (Mahajan et al., 2022, Adhikari et al., 2022). However, some researchers argued that pregnant women may not show mild symptoms when they were infected during the Omicron period in view of relatively low vaccination rates compared to the general population (Knight and Vousden, 2022). Moreover, pregnant women still have concerns about side effects, risk of miscarriage, and adverse effects on the fetus after vaccination given the limited data on vaccine safety (Levy et al., 2021, Rawal et al., 2022). Report of declining efficacy of COVID-19 vaccines also negatively impacts vaccine uptake in pregnant women (Birol Ilter et al., 2022a). Therefore, it is essential to comprehensively investigate the severity of maternal infection during the Omicron pandemic, and compare clinical outcomes after breakthrough infection in pregnant women with different vaccination statuses.

2. Clinical severity and pregnancy outcomes in pregnant women during the Omicron period

The disease severity and pregnancy outcomes in infected pregnant women vary between different viral variants. Specifically, the incidence of moderate and severe disease (5.1% vs. 3.8% vs. 15.6%, respectively), ICU admission (4.2% vs. 2.6% vs. 12.9%, respectively), and maternal mortality (0.3% vs. 0.4% vs. 4.9%, respectively) were lower during the Pre-Delta and Omicron period compared with during the Delta period ( Table 1). This may be because Delta infection is correlated with higher viral loads and greater infectivity. Concretely speaking, the peak viral load of Delta increases more than 1000 times compared to the wild-type SARS-CoV-2 strain (Wang et al., 2021b). Besides, Delta is 40–60% more transmissible than Alpha and almost twice as infectious as the wild-type SARS-CoV-2 strain (Hagen, 2021). Notably, the rate of adverse pregnancy outcomes, especially stillbirth (0.9% vs. 0.7% vs. 3.4%, respectively), was lower in Pre-Delta and Omicron period than in Delta period (Table 1). The placental pathology from two stillborns delivered to mothers with COVID-19 showed typical features of placentitis: the triad of histiocytic intervillositis, increased perivillous fibrin, and villous trophoblastic necrosis (Shook et al., 2022). Similarly, Schwartz et al. (2022) evaluated placentas from 64 stillborn fetuses and 4 neonatal deaths and found that all 68 placentas had increased fibrin deposition and villous trophoblastic necrosis and 66 had chronic histiocytic intervillositis (Schwartz et al., 2022). These suggest that the occurrence of stillbirth is related to inflammatory changes in the placenta. It’s worth noting that pregnant women with mild symptoms may also suffer severe placental inflammation and damage (Guan et al., 2022). Thus, although Omicron infection causes milder symptoms in pregnant women compared with Delta, its impact on pregnancy outcomes cannot be ignored. Pregnant women had a significantly higher incidence of asymptomatic disease (70.9% vs. 31.9%) and a lower proportion of critical disease (0 vs. 1.4%) during the Omicron period than Pre-Delta period (Table 1). This seems to indicate that Omicron is less virulent and may cause less severe symptoms than previous variants in pregnant women. However, the incidence of moderate and severe disease (5.1% vs. 3.8%), maternal mortality (0.3% vs. 0.4%), pregnancy loss (3.7% vs. 2.3%), preterm delivery (9.3% vs. 11.3%), stillbirth (0.9% vs. 0.7%), preeclampsia/eclampsia (7.0% vs. 6.8%), and gestational hypertension (5.2% vs. 4.9%) were similar between the Pre-Delta and Omicron period. Notably, available data had indicated that pregnant women infected with Pre-Delta were at higher risk for ICU admission (4.2% vs. 1.0%), maternal mortality (0.3% vs. 0), and preterm delivery (9.3% vs. 4.6%) compared with non-infected pregnant women (Table 1). Moreover, the proportion of pregnant women who received one or more doses of vaccine in the Omicron period was higher than that in the Pre-Delta period (36.0% vs. 0.1%) (Table 1). 70–80% of the CD4 and CD8 T cell response to Omicron spike was maintained across people vaccinated with Ad26. COV2. S or BNT162b2 vaccine, indicating that the T cell response induced by vaccination would cross recognize this variant (Keeton et al., 2022). What’s more, Fc-effector functional antibodies elicited by vaccine can induce antibody-mediated phagocytosis, complement deposition, and natural killer cell activation, providing additional disease prevention (Alter et al., 2021, Gorman et al., 2021). Thus, it is necessary to consider that previous vaccination may provide some protection against severe and symptomatic infections when comparing results across periods. Additionally, the severity of the disease may also be confounded by the immunity from previous infections. The response of IgG induced by natural infection to spike protein was relatively stable over six months (Dan et al., 2021). The use of antiviral therapy during Omicron period can also affect disease severity, resulting in milder symptoms (Flisiak et al., 2022). Hence, the virulence of Omicron may be comparable to or even higher than that of the Pre-Delta variant in pregnant women.

Table 1.

Disease severity and pregnancy outcomes in pregnant women infected with different SARS-CoV-2 variants.

Variant epoch
(Period covered)		 Country Pregnancy Unvaccinated COVID-19 severity
 Pregnancy outcomes
 Pregnancy complications
 Reference
Asymptomatic Symptomatic
 Admitted to ICU Maternal death Pregnancy loss Preterm delivery Stillbirth Neonatal death HELLP Preeclampsia/Eclampsia Gestational hypertension
Mild Moderate Severe Critical
Pre-Delta
(03/20–09/20)		 US 6550 (Diagnosed) 100% (6550/6550) NP 4.5% (293/6550) 0.1% (9/6550) NP 4.8% (315/6550) 1.0% (63/6550) NP 9.4% (616/6550) 5.3% (350/6550) (Ko et al., 2021)
482921
(Not diagnosed)		 100% (482921/482921) – 1.5% (7389/482921) 0 (32/482921) NP 3.6% (17392/482921) 0.7% (3439/482921) NP 6.8% (33078/482921) 6.6% (31787/482921)
Pre-Delta
(01/04/20–15/05/20)		 India 141
(Diagnosed)		 100% (141/141) NP NP 2.1% (3/141) 4.3% (6/141) NP NP NP 1.4% (2/141) NP NP (Nayak et al., 2020)
836
(Not diagnosed)		 100% (836/836) – NP 1.0% (8/836) 3.9% (33/836) NP NP NP NP
Pre-Delta
(04/20–08/20)		 India 633
(Diagnosed)		 100% (633/633) NP 1.3% (8/633) 0.3% (2/633) NP 0.9% (5/583) 1.4% (8/583) NP 1.5% (5/332) 2.1% (7/332) 7.8% (26/332) (Goyal et al., 2021)
1116
(Not diagnosed)		 100% （1116/1116） – 0.3% (3/1116) 0/1116 NP NP
Pre-Delta
(01/04/20–23/11/20)		 US 6380
(Diagnosed)		 100% (6380/6380) NP 3.3% (212/6380) 0.1% (9/6380) NP 7.2% (459/6380) 0.5% (34/6380) NP 0.5% (33/6380) 9.0% (572/6380) 6.0% (381/6380) (Jering et al., 2021)
400066
(Not diagnosed)		 100% (400066/400066) – 0.4% (1747/400066) 0 (20/400066) NP 5.8% (23234/400066) 0.3% (1289/400066) NP 0.2% (989/400066) 6.8% (27366/400066) 7.4% (29584/400066)
Pre-Delta
(03/20–10/20)		 18 countries 706
(Diagnosed)		 100% (706/706) 40.8% (288/706) 59.2% (418/706) 8.4% (59/706) 1.6% (11/706) NP 22.5% (159/706) NP NP 8.4% (59/706) 8.2% (58/706) (Villar et al., 2021)
1424
(Not diagnosed)		 100% (1424/1424) – 1.6% (23/1424) 0.1% (1/1424) NP 13.6% (194/1424) NP NP 4.4% (63/1424) 5.6% (80/1424)
Pre-Delta
(18/03/20–22/08/20)		 US 252
(Diagnosed)		 100% (252/252) 38.9% (98/252) 52.8% (133/252) 3.2% (8/252) 3.6% (9/252) 1.6% (4/252) NP NP 2.8% (7/252) 10.7% (27/252) 0/252 NP NP 10.3% (26/252) NP (Adhikari et al., 2020)
3122
(Not diagnosed)		 100% (3122/3122) – NP NP 2.8% (87/3122) 10.5% (328/3122) 0.6% (18/3122) NP NP 11.5% (359/3122) NP
Pre-Delta
(02/20–04/20)		 Asia 23 100% (23/23) 0/23 56.5% (13/23) 8.7% (2/23) 34.8% (8/23) 0/23 17.4% (4/23) 4.3% (1/23) NP 36.8% (7/19) NP NP 8.7% (2/23) 8.7% (2/23) NP (Antoun et al., 2020)
Pre-Delta
(01/04/20–01/12/20)		 Turkey 167 100% (167/167) NP 2.4% (4/167) 0.6% (1/167) 2.4% (4/167) 13.8% (23/167) NP NP 1.2% (2/167) 12.0% (20/167) NP (Aydin et al., 2021)
Pre-Delta
(03/20–07/20)		 France 126 100% (126/126) NP 16.7% (21/126) 0.8% (1/126) NP 42.1% (53/126) NP NP 0.8% (1/126) 9.5% (12/126) 1.6% (2/126) (Keita et al., 2021)
Pre-Delta
(03/03/20–11/05/20)		 US 141 100% (141/141) 31.2% (44/141) 58.2% (82/141) 6.4% (9/141) 4.3% (6/141) 3.5% (5/141) 0.7% (1/141) NP 3.8% (3/80) 0/80 0/80 1.3% (1/77) 15.6% (12/77) 5.2% (4/77) (Grechukhina et al., 2020)
Pre-Delta
(02/04/20–31/01/21)		 India 1143 100% (1143/1143) 85.8% (981/1143) 11.8% (135/1143) 2.4% (27/1143) 0/1143 2.4% (27/1143) 0.7% (8/1143) 2.7% (22/807) 8.3% (67/807) 1.5% (12/807) NP NP 5.8% (64/1103) 4.8% (53/1103) (Mahajan et al., 2022)
Pre-Delta
(22/03/20–31/05/21)		 US 224 100% (224/224) 46.4% (104/224) 40.6% (91/224) 12.9% (29/224) 8.0% (18/224) 0.4% (1/224) NP 33.0% (30/91) 6.6% (6/91) NP NP 23.1% (21/91) NP (Seasely et al., 2021)
Pre-Delta
(20/01/20–24/03/20)		 China 116 100% (116/116) 23.3% (27/116) 76.7% (89/116) 6.9% (8/116) 0/116 1.0% (1/100) 21.0% (21/100) NP 1.0% (1/100) NP 3.4% (4/116) 4.3% (5/116) (Yan et al., 2020)
Pre-Delta
(04/20–08/20)		 Turkey 75 100% (75/75) 12.0% (9/75) 65.3% (49/75) 21.3% (16/75) 1.3% (1/75) 0/75 2.7% (2/75) 0/75 14.6% (6/41) 26.8% (11/41) 2.4% (1/41) NP NP (Damar Cakirca et al., 2021)
Pre-Delta
(03/20–11/20)		 Saudi Arabia 288 100% (288/288) 14.2% (41/288) 85.8% (247/288) 3.8% (11/288) 0.3% (1/288) NP 15.2% (31/204) NP 0/204 NP 2.0% (4/204) NP (Al-Matary et al., 2021)
Pre-Delta
(01/03/20–14/04/20)		 UK 427 * 100% (427/427) NP 9.6% (41/427) 1.2% (5/427) 1.5% (4/266) 24.8% (66/266) 1.1% (3/266) 0.8% (2/266) NP (Knight et al., 2020)
Pre-Delta
(14/03/20–14/04/20)		 Spain 60 100% (60/60) 25.0% (15/60) 70.0% (42/60) 5.0% (3/60) 1.7% (1/60) 0/60 NP 8.7% (2/23) NP NP 1.7% (1/60) 5.0% (3/60) NP (Pereira et al., 2020)
Pre-Delta
(11/03/20–10/09/20)		 Turkey 533 100% (533/533) 0/533 95.5% (509/533) 3.2% (17/533) 0.9% (5/533) 0.4% (2/533) 1.3% (7/533) 0.4% (2/533) 9.0% (13/144) 15.3% (22/144) NP NP NP 0.9% (5/533) 0.8% (4/533) (Sahin et al., 2021)
Pre-Delta
(11/03/20–20/02/21)		 Turkey 1416 100% (1416/1416) 0/1416 93.4% (1322/1416) 4.6% (65/1416) 1.0% (14/1416) 1.1% (15/1416) 1.8% (26/1416) 0.4% (6/1416) 4.6% (58/1262) 18.1% (228/1262) NP NP NP 1.1% (15/1416) 0.9% (13/1416) (Sahin et al., 2022)
Pre-Delta
(13/03/20–27/03/20)		 US 43 100% (43/43) 0/43 86.0% (37/43) 0/43 9.3% (4/43) 4.7% (2/43) 4.7% (2/43) NP NP 5.6% (1/18) NP NP NP (Breslin et al., 2020)
Pre-Delta
(20/01/20–31/01/20)		 China 9 100% (9/9) NP 0/9 NP NP 0/9 0/9 44.4% (4/9) 0/9 0/9 NP 11.1% (1/9) 11.1% (1/9) (Chen et al., 2020a)
Pre-Delta
(01/03/20–14/04/20)		 France 617 100% (617/617) 19.4% (120/617) 74.9% (462/617) 5.7% (35/617) NP 0.2% (1/617) NP 27.6% (50/181) NP 0.6% (1/181) NP 3.4% (21/617) (Kayem et al., 2020)
Pre-Delta
(08/12/19–20/03/20)		 China 118 100% (118/118) 0/118 92.4% (109/118) 0/118 6.8% (8/118) 0.8% (1/118) NP 0/118 11.7% (9/77) 18.2% (14/77) NP 0/77 NP (Chen et al., 2020b)
Pre-Delta
(20/01/20–10/02/20)		 China 15 100% (15/15) 13.3% (2/15) 86.7% (13/15) NP 0/15 0/11 27.3% (3/11) 0/11 0/11 NP (Liu et al., 2020)
Pre-Delta
(01/03/20–22/08/20)		 US 598 * 100% (598/598) 54.5% (326/598) 45.5% (272/598) 7.4% (44/598) 0.3% (2/598) 2.2% (10/458) 12.2% (56/458) NP 0.4% (2/458) NP 12.0% (70/581) (Delahoy et al., 2020)
Pre-Delta
(01/03/20–10/05/20)		 US 149 100% (149/149) NP 5.4% (8/149) 0/149 NP 10.7% (16/149) 2.0% (3/149) 0.7% (1/149) NP NP 11.4% (17/149) (Verma et al., 2020)
Pre-Delta
(15/03/20–15/04/20)		 US 68 100% (68/68) 32.4% (22/68) 67.6% (46/68) NP 0/68 1.8% (1/56) 16.1% (9/56) NP NP NP 5.5% (3/55) NP (London et al., 2020)
Pre-Delta
(24/01/20–19/02/20)		 China 8 100% (8/8) 0/8 62.5% (5/8) 0/8 37.5% (3/8) 37.5% (3/8) 0/8 0/6 50.0% (3/6) 16.7% (1/6) 16.7% (1/6) NP 12.5% (1/8) NP (Huang et al., 2020)
Pre-Delta
(15/01/20–15/03/20)		 China 34 100% (34/34) 14.7% (5/34) 85.3% (29/34) 2.9% (1/34) NP 14.8% (4/27) 18.5% (5/27) NP 0/27 NP 2.9% (1/34) (Xu et al., 2020b)
Pre-Delta
(03/20–01/22)		 Turkey 783 100% (783/783) NP 13.0% (102/783) 4.1% (32/783) 1.3% (10/783) NP (Tekin et al., 2022)
Pre-Delta
(12/20–06/21)		 US 185 85.4% (158/185) 37.3% (69/185) 58.9% (109/185) 3.8% (7/185) 2.7% (5/185) NP NP (Eid et al., 2022b)
Pre-Delta
(15/03/20–31/07/20)		 Spain 105 NP 35.2% (37/105) 64.8% (68/105) 4.8% (5/105) 0/105 NP 20.0% (21/105) NP NP NP 0/105 NP (Carrasco et al., 2021)
Pre-Delta
(21/01/20–09/02/20)		 China 5 100% (5/5) NP NP 0/5 0/5 40.0% (2/5) NP 0/5 NP (Xu et al., 2020a)
Pre-Delta
(01/02/20–30/04/20)		 22 countries 388 NP 24.2% (94/388) 75.8% (294/388) 11.1% (43/388) 0.8% (3/388) 2.3% (6/266) 26.3% (70/266) 2.3% (6/266) 1.9% (5/266) NP (The WAPM World Association of Perinatal Medicine Working Group on COVID-19, 2021)
Total 22526
(Diagnosed) 		99.9% (22006/22033) 31.9% (2282/7156) 63.8% (2394/3752) 5.1% (184/3603) 1.4% (59/4220) 4.2% (890/21301) 0.3% (77/22210) 3.7% (151/4089) 9.3% (1783/19169) 0.9% (137/15491) 0.7% (13/1839) 0.6% (47/7306) 7.0% (772/11057) 5.2% (914/17497) –
889485
(Not diagnosed) 		100% (889485/889485) – 1.0% (9162/885527) 0 (61/886363) 3.0% (120/3958) 4.6% (41148/887533) 0.5% (4746/886109) NP 0.2% (989/400066) 6.9% (27725/403188) 6.9% (61451/884411) –
Delta
(01/02/21–10/12/21)		 India 597 100% (597/597) 60.8% (363/597) 24.8% (148/597) 14.4% (86/597) 0/597 14.7% (88/597) 6.4% (38/597) 7.9% (30/381) 11.0% (42/381) 3.4% (13/381) NP NP 6.7% (36/535) 8.6% (46/535) (Mahajan et al., 2022)
Delta
(01/07/21–18/08/21)		 US 69 NP 15.9% (11/69) 47.8% (33/69) 36.2% (25/69) 29.0% (20/69) 1.4% (1/69) NP 78.6% (22/28) 3.6% (1/28) NP NP 17.9% (5/28) NP (Seasely et al., 2021)
Delta
(20/02/21–15/09/21)		 Turkey 519 100% (519/519) 1.0% (5/519) 76.7% (398/519) 12.7% (66/519) 4.2% (22/519) 5.4% (28/519) 12.9% (67/519) 2.9% (15/519) 14.5% (33/228) 38.2%
(87/228)		 NP NP NP 1.3% (7/519) 1.3% (7/519) (Sahin et al., 2022)
Delta
(03/20–01/22)		 Turkey 243 100% (243/243) NP 17.7% (43/243) 11.5% (28/243) 7.0% (17/243) NP (Tekin et al., 2022)
Delta
(07/21–16/12/21)		 US 161 75.8% (122/161) 21.7% (35/161) 69.6% (112/161) 8.7% (14/161) 6.2% (10/161) NP NP (Eid et al., 2022b)
Delta
(07/21–08/21)		 US 61 93.4% (57/61) 37.7% (23/61) 62.3% (38/61) 4.9% (3/61) NP NP 27.3% (9/33) 3.0% (1/33) NP NP 4.9% (3/61) NP (Wang et al., 2021a)
Delta
(07/21–10/21)		 US 99 82.8% (82/99) 19.2% (19/99) 57.6% (57/99) 23.2% (23/99) 9.1% (9/99) 2.0% (2/99) NP 21.6% (21/97) NP NP 11.3% (11/97) (Eid et al., 2022a)
Delta
(09/06/21–27/12/21)		 Turkey, UK 339 100% (339/339) NP 5.3% (18/339) NP 25.2% (31/123) 3.3% (4/123) NP NP 2.4% (8/339) NP (Birol Ilter et al., 2022b)
Total 2088 97.0% (1959/2019) 30.3% (456/1506) 49.6% (603/1215) 15.6% (174/1116) 2.5% (28/1116) 12.9% (225/1749) 4.9% (91/1866) 10.3% (63/609) 23.8% (212/890) 3.4% (19/565) NP NP 4.0% (59/1482) 5.0% (53/1054) –
Omicron
(18/12/21–19/01/22)		 India 288 91.3% (263/288) 54.5% (157/288) 45.1% (130/288) 0.3% (1/288) 0/288 2.4% (7/288) 0/288 4.6% (9/196) 6.1% (12/196) 1.0% (2/196) NP NP 6.8% (18/263) 4.9% (13/263) (Mahajan et al., 2022)
Omicron
(03/20–01/22)		 Turkey 39 100% (39/39) NP 5.1% (2/39) 5.1% (2/39) 2.6% (1/39) NP (Tekin et al., 2022)
Omicron
(17/12/21–01/22)		 US 126 53.2% (67/126) 38.1% (48/126) 58.7% (74/126) 3.2% (4/126) 2.4% (3/126) NP NP (Eid et al., 2022b)
Omicron
(27/12/21–14/02/22)		 Turkey, UK 77 100% (77/77) NP 1.3% (1/77) NP 8.3% (3/36) 0/36 NP NP 6.5% (5/77) NP (Birol Ilter et al., 2022b)
Omicron
(15/12/21–14/03/22)		 UK 3699 * 61.6% (1886/3064) 73.3% (2713/3699) NP 3.9% (144/3699) NP 3.0% (30/986) 0.4% (4/986) 2.2% (62/2841) 11.7% (324/2764) 0.7% (19/2841) 0.4% (10/2841) NP (Engjom et al., 2022)
Omicron
(27/12/21–01/02/22)		 Turkey, UK 135 38.5% (52/135) 96.3% (130/135) 3.7% (5/135) 0/135 1.5% (2/135) 0/135 NP (Birol Ilter et al., 2022a)
Omicron
(17/01/22–07/03/22)		 Korea 94 68.1% (64/94) 89.4% (84/94) 10.6% (10/94) 0/94 0/94 NP NP 7.1% (3/42) NP NP NP (Kim et al., 2022)
Total 4458 64.0% (2448/3823) 70.9% (2918/4113) 45.1% (130/288) 3.8% (160/4216) 0/517 2.6% (44/1668) 0.4% (6/1525) 2.3% (71/3037) 11.3% (342/3038) 0.7% (21/3073) 0.4% (10/2841) NP 6.8% (23/340) 4.9% (13/263) –
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Note: ICU, intensive care unit; NP, not provided; -, not available; HELLP, the clinical presentation of hemolysis, elevated liver enzymes, low platelet count. *Some pregnant women had missing data.

3. Safety and effectiveness of COVID-19 vaccination in pregnancy

Although adverse events such as fatigue, fever or chills, injection-site pain and headache were reported after vaccination of pregnant women, these symptoms were not severe. Moreover, their rates were not significantly different or even lower than those reported in the general population (Kadali et al., 2021, Kachikis et al., 2021). According to the Centers for Disease Control and Prevention, most effects were temporary and rarely lasted beyond three days (Centers for Disease Control and Prevention, 2022a). Additionally, the proportions of adverse pregnancy and neonatal outcomes (e.g., preterm birth, neonatal death, etc.) of pregnant women who received the COVID-19 vaccine were similar to those reported in pregnant women before the COVID-19 pandemic (Shimabukuro et al., 2021). Given that the changes in the provision of healthcare services and the behavior of pregnant women may be altered by the indirect effects of the pandemic, it is important to compare vaccinated pregnant women with a contemporaneous control group. In fact, the vaccinated pregnant women did not have a significantly increased incidence of adverse pregnancy and neonatal outcomes compared with unvaccinated pregnant women in the context of the COVID-19 pandemic (Blakeway et al., 2022, Theiler et al., 2021). Bookstein Peretz et al. (2021) reported that the rate of vaginal bleeding after the second dose of vaccine in early pregnancy was only 3.8%, which is very low compared with the previously accepted rate of 16–27% (Bookstein Peretz et al., 2021, Hasan et al., 2009). Moreover, there were no increased rates of decidual arteriopathy, fetal vascular malperfusion, low-grade chronic villitis, or chronic histiocytic intervillositis among those who received the COVID-19 vaccine during pregnancy compared with unvaccinated pregnant individuals (Shanes et al., 2021). Thus, the risk of obstetric complications and abnormal placental development and function after COVID-19 vaccination appears to be negligible.

Pregnant women can develop immune responses after COVID-19 vaccination with immunogenicity comparable to that observed in the general population. What’s more, the protective immunoglobulins during pregnancy can effectively transfer across the placenta to the fetus (Gray et al., 2021). A prospective cohort study found that the median level of IgG antibodies at birth was 1185.2 AU/mL for parturient women vaccinated with BNT162b2 and 3315.7 AU/mL for neonates, with neonatal titers measuring approximately 2.6 times higher than maternal titers (Kugelman et al., 2022). This higher antibody level appears to provide strong protection against SARS-CoV-2 infection during the first months of infancy. In fact, epidemiological evidence has existed that infants born to mothers who received the two-dose mRNA vaccination series during pregnancy had a 61% reduced risk of SARS-CoV-2 hospitalization in the first six months of life (Halasa et al., 2022). Moreover, we made Table 2 to summarize the effect of COVID-19 vaccination status on maternofetal outcomes in pregnant women with breakthrough infections during the Omicron period (Birol Ilter et al., 2022a, Tekin et al., 2022, Eid et al., 2022b, Engjom et al., 2022). Although there was no difference in the proportion of moderate and severe disease between the unvaccinated group and the one dose group, the second dose or booster vaccination exhibited a strong protective effect (Table 2). Specifically, the incidence rate of moderate and severe disease in infected pregnant women who received the second dose or booster was reduced. What's more, none of the cases in these two populations died. However, pregnant women who have vaccinated and who have not vaccinated had a similar proportion of pregnancy loss, stillbirth, and admission to the neonatal unit after being infected. Some bias may exist in this outcome in view of the small cumulative number of subjects. Hence, larger multicentre trials and sample analyses are required to generate convincing results.

Table 2.

Clinical severity and maternofetal outcomes of infected pregnant women with different vaccination statuses during the Omicron wave.

Vaccination status Geographic area of focus Pregnancy Clinical severity
 Pregnancy outcomes
 Reference
Asymptomatic Mild Moderate Severe Critical Maternal death Pregnancy loss Stillbirth Admission to neonatal unit
Unvaccinated Turkey 39 NP NP NP 5.1% (2/39) 2.6% (1/39) NP NP NP (Tekin et al., 2022)
US 67 59.7% (40/67) 49.3% (33/67) 6.0% (4/67) NP NP NP NP (Eid et al., 2022b)
UK 1886 74.1% (1397/1886) NP 4.9% (93/1886) NP 0.1% (3/1886) 1.9% (28/1479) 0.7% (10/1479) 9.5% (140/1479) (Engjom et al., 2022)
Turkey, UK 52 90.4% (47/52) 9.6% (5/52) 0/52 0/52 NP NP NP (Birol Ilter et al., 2022a)
1 dose UK 333 67.9% (226/333) NP 4.2% (14/333) NP 0.3% (1/333) 1.2% (3/260) 1.2% (3/260) 9.6% (25/260) (Engjom et al., 2022)
2 doses US 59 30.5% (18/59) 69.5% (41/59) 0/59 0/59 NP NP NP (Eid et al., 2022b)
UK 650 70.2% (456/650) NP 2.9% (19/650) NP 0/650 2.1% (10/487) 1.0% (5/487) 11.3% (55/487) (Engjom et al., 2022)
Turkey, UK 70 100% (70/70) 0/70 0/70 0/70 0/70 NP NP NP (Birol Ilter et al., 2022a)
3 doses UK 195 71.8% (140/195) NP 1.5% (3/195) NP 0/195 3.3% (5/151) 0/151 7.9% (12/151) (Engjom et al., 2022)
Turkey, UK 13 100% (13/13) 0/13 0/13 0/13 0/13 NP NP NP (Birol Ilter et al., 2022a)
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Note: NP, not provided.

4. Barriers and responses to COVID-19 vaccination in pregnant women

The WHO, the Centers for Disease Control, and the American College of Obstetricians and Gynecologists have recommended that pregnant women should receive enough doses of the COVID-19 vaccine in a timely manner (World Health Organization, 2022a, Centers for Disease Control and Prevention, 2022c, The American College of Obstetricians and Gynecologists, 2022b). However, the current low vaccination uptake is a complex issue. In addition to concerns about safety and effectiveness, it also involves recommendations of health care professionals, institutional trust, and low knowledge of vaccines. Healthcare providers are known to be important long-term partners in the recommendation and safe administration of vaccines (Centers for Disease Control and Prevention, 2022b, The American College of Obstetricians and Gynecologists, 2022a). Attitudes toward immunization in pregnant women are often aligned with the provider’s recommendation of vaccination (Shavell et al., 2012). Thus, it is not difficult to understand that they are still the most trusted influencers of vaccination decisions in this Omicron wave. However, some obstetricians and gynecologists, and other health care providers are not leading by example in vaccination. Generally speaking, if they are not vaccinated, they will not encourage eligible patients to be vaccinated (Silverman and Greif, 2001). Hence, education and policy-based interventions should be implemented to ensure that healthcare workers are vaccinated with the available COVID-19 vaccines. Furthermore, all of them must receive ongoing training and guidance as new recommendations regarding vaccines in pregnancy evolve. Institutional trust is a distal factor influencing pregnant women’s vaccination hesitancy and is part of evolving conspiracy theories that emphasizes distrust of government organizations (Zimand-Sheiner et al., 2021). Research on exposure to vaccine-related information reveals that even if trust in vaccine information is positively correlated with attitudes and behavior, it is not enough when relevant institutions are mistrusted (Park et al., 2021). Thus, the government needs to put more effort into communication with those who have low levels of trust in institutions. Moreover, public health practitioners and government officials should have more professional knowledge and authority, striving to promote an image of public trust and sincerity. Information overload, misinformation, and myths on the internet are also important barriers to pregnant women receiving the vaccine (Dzinamarira et al., 2021). Gencer et al. (2022) reported that women who used mass media or the internet as their primary source of information showed higher levels of hesitation (Gencer et al., 2022). Hence, all healthcare professionals have a responsibility to participate in the development of strategies to provide scientific evidence before anti vaccine and other similar activities which promote false information about the safety and effectiveness of vaccines.

5. Conclusion

The severity of disease and pregnancy outcomes in pregnant women with COVID-19 vary with different variants. Although infected pregnant women during the Omicron period were at lower risk for ICU admission, maternal mortality, and stillbirth than during Delta period, they had a similar proportion of moderate and severe disease, maternal mortality, pregnancy loss, preterm delivery, stillbirth, preeclampsia/eclampsia, and gestational hypertension compared with infected pregnant women during the Pre-Delta period. Considering the effects of immune status and availability of antiviral treatment on disease severity, the virulence of Omicron in pregnant women may be comparable to or even higher than that of Pre-Delta variant.

Adverse events such as fatigue, fever or chills, injection-site pain and headache were reported in pregnant women after vaccination. However, these symptoms were not severe. Moreover, there was no increase in adverse maternal-fetal outcomes, obstetric complications, and abnormal placental development and function among vaccinated pregnant women compared with unvaccinated women. COVID-19 vaccines can generate robust humoral immunity in pregnant women, with immunogenicity and reactogenicity similar to that observed in general population. Additionally, protective immunoglobulins after vaccination during pregnancy can be delivered across the placenta to the fetus, which can provide protection against COVID-19-related hospitalization. Given that there was no difference in the incidence of moderate and severe disease between infected women vaccinated with one dose and those without vaccination, pregnant women should receive second dose or booster to obtain adequate protection. Notably, recommendations of health care professionals, institutional trust, and low knowledge of vaccines also affect willingness of pregnant women to receive a COVID-19 vaccine. Thus, the government was advised to take public health measures to promote vaccination programs. Moreover, the clinicians should encourage individuals who are planning to become pregnant to complete their vaccination series before conception to ensure they are protected. Considering that maternal vaccination initiated in the early second trimester of pregnancy may bring the best innate immunity against SARS-CoV-2 infection for the newborn, vaccination during this window is also a good option.

Funding

This work was supported by the Natural Science Foundation of Shandong Province (Grant No. ZR2020QC100).

Acknowledgments

None.

Authors’ contributions

All authors contributed to writing, editing, and revising of the manuscript.

Conflict of interest

The authors declare no conflict of interest.

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