Safety, Efficacy, and Effectiveness of Maternal Vaccination against Respiratory Infections in Young Infants

• Abstract
• Pertussis
• Maternal Pertussis Vaccine
• Safety
• Immunogenicity
• Efficacy and Effectiveness
• Other Considerations
• Influenza
• Maternal Influenza Vaccine
• Safety
• Immunogenicity
• Efficacy and Effectiveness
• Respiratory Syncytial Virus
• Maternal Respiratory Syncytial Virus Vaccine
• Safety
• Immunogenicity
• Efficacy and Effectiveness
• Other Considerations
• Severe Acute Respiratory Syndrome Coronavirus-2 Vaccine
• Maternal COVID-19 Vaccine
• Safety
• Immunogenicity
• Efficacy and Effectiveness
• Considerations for Maternal Vaccination Implementation
• Addressing Vaccine Hesitancy
• Improving Delivery and Administration Pathways
• Engaging all Stakeholders
• Conclusion
• References

Abstract

Lower respiratory tract infection (LRTI) is a major cause of neonatal morbidity and mortality worldwide. Maternal vaccination is an effective strategy in protecting young infants from LRTI, particularly in the first few months after birth when infant is most vulnerable, and most primary childhood vaccinations have not been administered. Additionally, maternal vaccination protects the mother from illness during pregnancy and the postnatal period, and the developing fetus from adverse outcomes such as stillbirth and prematurity. In this paper, we review the safety, efficacy, and effectiveness of maternal vaccines against LRTIs, such as pertussis, influenza, coronavirus disease 2019, and respiratory syncytial virus.

Lower respiratory tract infections (LRTIs) remain the leading cause of death among children aged 1 to 59 months, responsible for more than 502,000 deaths in this age group in 2021.[1] Approximately 40% of childhood LRTI-related deaths occur in the first 6 months of life.[2] Respiratory syncytial virus (RSV) is the dominant cause of LRTI among hospitalized infants, being the etiological agent in 80% of bronchiolitis and 20 to 45% of bronchopneumonia cases.[3] [4] [5] [6] [7] [8] In the Pneumonia Etiology for Child Health Study (PERCH) conducted in seven low- and middle-income countries (LMICs) in Africa and Southeast Asia, other common pathogens attributed to causing pneumonia in infants 1 to 6 months of age included viruses (human metapneumovirus [7.3%], parainfluenza I–IV [6.9%], rhinovirus [2.5%], influenza A/B/C [1.4%]) and bacteria (Mycobacterium tuberculosis [6.9%], Streptococcus pneumoniae [4.1%], Haemophilus influenzae [5.7%], Bordetella pertussis [1.8%]).[8]

Neonates and young infants are particularly vulnerable to infectious diseases due to naïve immune systems.[9] Consequently, many childhood vaccines are approved for use in children over 6 weeks of age and often require more than two priming doses before adequate immunity is achieved.[10] [11] [12] Vaccination of the pregnant woman has been effectively deployed in protecting newborns and young infants (<6 months of age) against neonatal tetanus, pertussis, influenza, coronavirus disease 2019 (COVID-19), and, more recently, against RSV.[13] Furthermore, maternal vaccines protect the pregnant women and developing fetus. Structural, physiological, and immunological changes to the cardiovascular and respiratory system during pregnancy increases susceptibility to vaccine preventable diseases in pregnant women.[14] [15] Historically, the increased maternal susceptibility to severe infectious disease was recorded as far back as the 19th century in relation to smallpox and measles outbreaks.[16] [17] Similarly, maternal infection with pandemic strains of influenza (Spanish Flu) had higher rates of morbidity and mortality.[18] [19] [20] More recently, pregnant women infected with severe acute respiratory syndrome coronavirus type 2 (SARS-CoV-2) had more severe illness and a higher risk of adverse fetal outcomes, including preterm delivery and stillbirth.[21] Vaccinating pregnant women can reduce this burden of disease by conferring direct benefit to mothers, including reducing the risk of respiratory illness and preventing adverse fetal outcomes such as stillbirth or preterm labor.[22] [23] [24]

History of Vaccines in Pregnancy

The benefit of maternal vaccination in protecting both mother and infant was serendipitously discovered in 1879, when infants born to pregnant women vaccinated against smallpox were shown to be immune to the disease during early life.[25] The first clinical trial of vaccines in pregnant women was undertaken in Papua New Guinea in 1961, which demonstrated the efficacy of two or more doses of fluid formalinized tetanus toxoid vaccine in preventing neonatal tetanus.[26] However, the unforeseen teratogenicity of thalidomide in pregnant women swiftly resulted in the U.S. Food and Drug Administration (FDA) excluding pregnant women and those of childbearing potential from further drug and vaccine trials in 1977.[27]

In 1989 the World Health Organization (WHO) launched the flagship maternal and neonatal tetanus elimination program, with maternal vaccination proving crucial to the success of the program.[28] Subsequently, the FDA overturned their decision for women of childbearing age to be excluded from clinical trials in 1993.[27] In 2010, joint efforts by several nongovernmental organizations, including the Bill and Melinda Gates Foundation (BMGF), coupled with emerging safety and efficacy data of influenza vaccination in pregnancy led to the WHO endorsing recommendation for influenza vaccination to all pregnant women.[29]

There is general consensus regarding the safety of killed or inactivated vaccines, protein subunit vaccines, toxoid-containing vaccines, conjugate vaccines, and, more recently, the messenger ribonucleic acid (mRNA) and nonreplicating viral vector vaccines in pregnant women.[30] [31] [32] [33] Vaccines that contain live attenuated viruses are generally contraindicated in pregnancy due to a theoretical risk of congenital infection and a potential increased risk of miscarriage.[34] Nevertheless, a risk–benefit analysis is deemed reasonable for the use of a live-attenuated vaccine where indicated. Vaccines currently recommended for pregnant women by the Centers for Disease Control and Prevention (CDC) include COVID-19 (any vaccine type), influenza (inactivated or recombinant), pertussis (acellular), and a bivalent subtype A/B RSV prefusion (RSVA/B-preF) vaccine (ABRYSVO).[35] Vaccines for pregnant women in the pipeline include those against group B streptococcus and Klebsiella pneumonia.[36] [37] Other pathogens earmarked for future maternal vaccine development include cytomegalovirus, malaria, human immunodeficiency virus (HIV), zika virus, and extra-intestinal Escherichia coli.[38]

Maternal and Fetal Immunity and the Influence of Antenatal Vaccination

Fetal and infant immune protection following the vaccination of pregnant women is primarily mediated via transplacental transfer of maternal immunoglobulin G (IgG) antibodies to the developing fetus. Maternal IgG antibodies are transferred across the placenta via syncytiotrophoblast cells to the developing fetus and could provide protection against pathogens to which the mother had previously developed immunity from either past infection or vaccination.[39] Following endocytosis from maternal circulation, IgG binds to neonatal fragment crystallizable receptors (FcRn), which are expressed on the internal endosomal surface of the placenta, under acidic pH.[40] The endosome is then transported to the fetal aspect of the syncytiotrophoblast where IgG antibodies dissociate from the FcRn at physiological pH.[40] IgG then passes through villous stroma and fetal capillary endothelium and enters fetal circulation as shown in [Fig. 1]. This process typically begins at the end of the first trimester of pregnancy, with transplacental fetal-to-maternal IgG ratios reaching approximately 50% by the end of the second trimester.[39] [41] A full-term infant can have IgG concentrations equal to or greater than the mother, whereas preterm infants have reduced concentrations of maternal IgG, making them more susceptible to vaccine-preventable diseases compared with term infants.[41] [42]

The transplacental transfer of IgG is affected by several factors, including chronic maternal infections, placental integrity, maternal immune status, IgG subtype and antigen-specificity, and infant gestational age and birthweight.[43] [44] Epitope-specific IgG concentrations have been associated with longer and more effective protection against the relevant pathogen in the young infant.[45] [46] Maternal vaccination aims to boost maternal antibody levels to enhance transplacental transfer of IgG to achieve protective levels in the newborn.

In this narrative we discuss the safety, immunogenicity, and effectiveness of vaccines currently licensed for use in pregnant women, with the aim of protecting young infants against respiratory illness, namely pertussis, influenza, COVID-19, and RSV.

Pertussis

Bordetella pertussis, a gram-negative coccobacillus, is endemic to all countries and infects approximately 24.1 million people worldwide annually, with an estimated 56,000 to 85,900 deaths in infants.[47] [48] Infant vaccination against pertussis has been a part of the Expanded Programme on Immunization since 1974, and globally, approximately 1.3 million pertussis-related deaths were estimated to have been averted in 2001.[49] Despite the success of the childhood pertussis immunization program, epidemic cycles still occur every 2 to 5 years.[50] The WHO estimates that 90% of pertussis cases occur in LMICs, with the African region accounting for 58% of cases.[47] [48] [51] Nevertheless, the incidence of pertussis and frequency of outbreaks have been increasing in high-income countries (HICs) including young infant and older age groups.[52] [53] This increase is partly attributed to the transitioning from whole-cell inactivated pertussis (wP) to acellular pertussis (aP) vaccines.[54] While 60% of pertussis infections occur in adults, 76 to 90% of deaths occur in the first 3 months of life, i.e., in infants too young to have been fully vaccinated against pertussis.[48] [55] [56]

Vaccinating pregnant women is an effective strategy to reduce the burden of pertussis in vulnerable young infants.[48] While, wP vaccines are not licensed for use in pregnant women, several aP vaccines are available for use in pregnant women, which include pertussis toxoid (PT) together with one or more of adhesion proteins of filamentous hemagglutinin, pertactin (PRN), and fimbriae (FIM) types 2 and 3 (FIM2/3).[57] [58] Most HICs recommend vaccination of pregnant women with aP vaccines that include tetanus and diphtheria toxoids (Tdap) in each pregnancy.[59] [60]

Maternal Pertussis Vaccine

Safety

The first large prospective study on the safety of aP vaccine in pregnant women was conducted in the United Kingdom, following an upsurge of pertussis cases toward the end of 2011, which lead the United Kingdom's Joint Committee on Vaccination and Immunization to recommend a temporary maternal vaccination program for pregnant women between 28 and 38 weeks' gestation.[61] This study included 20,074 pregnant women who received the aP vaccine (Repevax; Sanofi Pasteur MSD, Maidenhead, UK) and demonstrated no increased risk of severe adverse maternal or neonatal outcomes compared with historical rates.[62] A further longitudinal cohort study in the United States on 123,494 pregnant women with singleton pregnancies, also reported that Tdap (majority of doses were Adacel, Sanofi Pasteur) was safe in pregnant women, without any increase in risk of maternal hypertension, prematurity, or small for gestational age (SGA) babies, compared with expected population rates.[63] In a systematic review that included 1.4 million pregnant women, pertussis vaccination was, however, associated with an increased risk of medically attended fever within 3 days of vaccination in one study[64] (relative risk [RR]: 2.16; 95% confidence interval [CI]: 1.65–2.83).[65]

Immunogenicity

Although a serological correlate of protection against pertussis has not been definitively established, there is an association between higher maternal PT IgG and infant protection against pertussis.[66] [67] [68] [69] The pertussis-specific IgG levels in cord blood are generally higher than maternal levels in infants born to vaccinated women; however, they wane to undetectable levels as early as 4 months of life, necessitating the need for infant pertussis vaccination for ongoing protection.[70] The immunogenicity of aP vaccination in pregnant women may be influenced by whether the women received aP or wP during childhood.[71] Anti-pertussis toxin (PT) IgG following aP vaccination in the pregnant women was 50% lower in women vaccinated with aP compared with wP recipients in childhood (geometric mean concentrations, GMC: 17.3 vs. 36.4; GMC ratio, 0.475; 95% CI: 0.408–0.552).[71]

Efficacy and Effectiveness

Cohen and Scadron first demonstrated the efficacy of maternal vaccination with wP vaccines in a small study in the 1940s, where the incidence of pertussis was lower in infants born to vaccinated compared with unvaccinated women.[72] However, interest in the benefit of maternal vaccination with wP was limited, with the scientific community focusing rather on the effectiveness of infant vaccination with wP as a strategy to protect against pertussis in children.[73] The advent of aP vaccines soon replaced wP vaccines due to better reactogenicity and safety profiles. However, the effectiveness of aP vaccination is 62% (95% CI: 42–75%) at 4- to 7-year postvaccination, mandating aP booster doses every 5 to 10 years throughout adulthood.[74] [75] The waning pertussis immunity in unvaccinated women of childbearing age perpetuates the public health problem of an increase in pertussis infection in young infants.

Other Considerations

Although highly effective in protecting young infants against pertussis, maternal Tdap vaccination may interfere with subsequent immune response to some other vaccines administered to infants.[76] [77] A meta-analysis by Voysey et al of 32 studies on 7,630 infants across 17 countries demonstrated blunted antibody responses following childhood vaccination for 20 of 21 antigens contained in global immunization programs, including against aP, inactivated polio, diphtheria, and pneumococcal polysaccharide–protein (CRM197) conjugate vaccines.[78] For aP antigens, higher maternal antibody levels were inversely associated with infant immune responses.[78] [79] The clinical significance of the attenuated immune responses to some of the childhood vaccines, due to higher baseline antibodies derived from maternal vaccination, has not been elucidated.

Influenza

Pregnant women experience a disproportionately higher risk of influenza-related morbidity and mortality than the general population. The annual global incidence of influenza in pregnant women ranges between 483 and 1,097 per 10,000, whereas influenza-related hospitalizations range between 0.04 and 7.7 per 10,000 pregnancies.[80] During the 1918 H1N1 influenza pandemic, the case fatality rate was 27% in pregnant women compared with 2.5% in general adult population.[19] [81] A meta-analysis, including 186,656 individuals, reported that influenza infection in pregnant women was associated with a 7-fold (odds ratio: 6.8; 95% CI: 6.02–7.68) increased odds of hospitalization compared with their nonpregnant counterparts.[82]

There remains a paucity of data on the burden of influenza illness in pregnant women from LMICs.[80] In South Africa, between 1999 and 2009, the estimated mean annual seasonal influenza–associated mortality rates (per 100,000 person-years) in pregnant women was 12.6 compared with 7.3 in nonpregnant women (RR: 2.8, 95% CI: 1.7–3.9).[83] This may, in part, be attributable to the high prevalence of HIV infection in Sub-Saharan Africa. In pregnant and nonpregnant women with HIV, the influenza-associated mortality rate per 100,000 persons was 74.9 and 41.2, respectively, whereas rates in pregnant and nonpregnant women without HIV were 1.5 and 0.9, respectively.[83]

Pregnant women with influenza infection are also at increased risk of adverse pregnancy and neonatal outcomes. A systematic review of 17 studies including 2,351,204 pregnant women reported that influenza infection in pregnant women increased the risk of stillbirth (RR: 3.62, 95% CI: 1.60–8.20), with a trend toward higher risk of preterm birth (RR: 1.17, 95% CI: 0.95–1.45) and SGA (RR: 1.10, 95% CI: 0.98–1.24).[84] Systematic reviews of H1N1 pandemic in 2009 showed that pregnant women with severe disease had higher rates of preterm delivery (risk ratio: 2.44, 95% CI: 1.81–3.30), infants born with low birth weight (RR: 2.28, 95% CI:1.81 − 2.87) and up to 4-fold odds of fetal death (adjusted odds ratio [aOR] 4.2, 95% CI: 1.4–12.4), particularly among women requiring hospitalization.[84] [85]

Among young infants, the burden of influenza remains proportionally low. A systematic review of studies from 15 HICs and 12 LMICs and upper-middle-income countries (UMICs) reported that laboratory confirmed seasonal influenza hospitalization rates ranged from 9.3 to 91.2 per 10,000 infants under 6 months of age.[86] In the PERCH, multisite international case–control study, influenza virus was only attributed as the cause of severe LRTI hospitalization in 1.4% (95% CI: 0.4–2.6) of infants 1 to 5 months of age.[5]

Vaccination of pregnant women against influenza is an effective strategy toward protecting mothers from severe illness, adverse fetal outcomes, and illness in infants less than 6 months of age.[87] A vaccine against influenza has been available since the 1940s, with the first large-scale trial demonstrating high efficacy against epidemics in the United States between 1942 and 1945.[88] In 1960, recommendations were made by public health authorities for the use of inactivated influenza vaccines (IIV) in pregnant women due to the higher risk of severe disease.[89] Nevertheless, it was not until 1997 that the CDC endorsed use of IIV in pregnant women aimed at protection of both the mother and their young infants.[90]

Maternal Influenza Vaccine

Safety

There is a broad, and growing, body of evidence to support the safety of influenza immunization in pregnancy. A systematic review of 40 studies using either seasonal IIVs or monovalent H1N1pdm09 vaccine in pregnant women found lower odds of preterm birth (aOR: 0.87; 95% CI: 0.78–0.96) and low birth weight babies (aOR: 0.82, 95% CI: 0.76–0.89) among vaccinated women compared with unvaccinated mothers.[91] In addition, there was no difference in congenital abnormality (aOR: 1.03; 95% CI: 0.99–1.07), SGA (aOR: 0.99, 95% CI: 0.94–1.04), and stillbirth (aOR: 0.84, 95% CI: 0.65–1.08).[91] Furthermore, longitudinal cohort studies evaluating the effect of in utero exposure to IIV have not identified any increased risk of neurocognitive delays, behavioral disorders (e.g., autism spectrum disorders), malignancies, and allergic conditions in offspring born to women who received IIV during pregnancy compared with those of unvaccinated women.[92] [93] [94]

Immunogenicity

The first randomized clinical trial (RCT) of IIV in pregnant women was undertaken in Bangladesh in 2004, where 340 mothers were randomly assigned to receive either trivalent influenza vaccine (IIV; Fluarix) or the 23-polysaccaride pneumococcal vaccine (Pneumovax).[95] This study, together with an RCT carried out in Nepal, found vaccinated women had significant hemagglutination–inhibition (HAI) titer increases −2 to 18-fold from prevaccination to delivery (HAI titers of ≥1:40 is indicative of seroprotection, while seroconversion from pre- to postvaccination requires a 4-fold increase in HAI titers).[95] [96] [97] Subsequently, two other RCTs carried out in South Africa and Mali found that titers increased by 9.4-, 6.0-, and 9.6-fold for A/H1N1, A/H3N2 and B/Victoria, respectively, 1 month following vaccination.[98] The South African study found 93, 78, and 96% seroprotection rates against A/H1N1pdm09, A/H3N2, and B/Victoria, respectively.[99] Immunogenicity was, however, reduced in pregnant women living with HIV (PWLWH). A meta-analysis of influenza vaccination demonstrated significantly lower GMCs among PWLWH compared with pregnant women without HIV (pooled geometric mean difference in HAI titers postvaccination −141.8 [95% CI: −194.9, −88.6; p < 0.0001]).[100]

Efficacy and Effectiveness

The efficacy and effectiveness of influenza vaccination has been well-established. The first RCT among pregnant women (in Bangladesh) showed a vaccine efficacy (VE) of 36% (95% CI: 4–57) against respiratory illness with fever in recipients of the trivalent influenza vaccine (TIV) compared with pneumococcal vaccine.[95] Subsequently, RCTs conducted in South Africa, Mali, and Nepal reported vaccine efficacies between 31% (95% CI: 10–56%) and 70% (95% CI: 42–86%) against PCR-confirmed influenza in pregnant women, respectively.[96] [99] [101]

More recently, a retrospective cohort study of 34,701 pregnant women in Western Australia reported that a seasonal trivalent vaccine in pregnant women was associated with 81% reduction of influenza-associated emergency department visits (adjusted hazards ratio, aHR: 0.19, 95% CI: 0.05–0.68) and 65% reduction in hospital admissions during the 2012/2013 vaccine season (aHR: 0.35, 95% CI: 0.13–0.97).[102] Furthermore, a larger multicenter study across four HICs, using integrated health records for approximately 19,450 pregnant women, found an overall adjusted effectiveness of 40% (95% CI: 12–59) against PCR-confirmed influenza-associated hospitalization.[103] A recent systematic review (2023) estimated that the effectiveness of IIV in pregnant women was 42% (RR: 0.58, 95% CI: 0.42–0.79) against laboratory-confirmed influenza in mothers.[104]

A pooled analysis of 9,800 infants reported the efficacy of maternal vaccination in preventing PCR-confirmed influenza in infants up to 6 months of age to be 36% (95% CI: 22–48%). However, studies have shown that antibodies passively transferred to infants had half-lives of 42 to 50 days.[95] [105] Waning protection was clearly seen as the pooled efficacy decreased from 56% (95% CI: 28–73) in infants within 2 months of life to 39% (95% CI: 11–58) between 2 and 4 months and finally 19% (19%; 95% CI: −9 to 40%) between 4 and 6 months.[106] Notably, influenza vaccine trials found a 20% reduction in all-cause severe pneumonia in infants less than 6 months who were born to women vaccinated with TIV during pregnancy. In South Africa, there was a 43% lower incidence rate of severe pneumonia in the IIV group versus the control group (incidence rate ratio (IRR): 0.57; 95% CI: 0.33–1.0).[107] These findings suggest possible protection against secondary bacterial infections following influenza infection.

Respiratory Syncytial Virus

RSV is the commonest cause of LRTI in infants. In 2019, an estimated 33 million cases of RSV LRTI, 3.6 million RSV-related hospitalizations and 101,400 deaths occurred in children under 5 years of age across the globe.[108] Of these cases, six million (18%) occurred in infants less than 6 months of age, with 1.4 million RSV-associated hospitalizations (39%) and 45,700 RSV-attributable deaths (45%) in this age group alone.[108] The overwhelming majority of infections (95%) and RSV-associated deaths (97%) occur in LMICs, with nearly half of the global burden of RSV disease occurring in infants in the first 6 months of life.[109]

RSV infection is less commonly seen in adults, with an estimated attack rate of 10% for RSV respiratory tract infection (RTI) in pregnant women in ambulatory care and an RSV hospitalization rate of approximately 2%.[110] There are limited data on perinatal outcomes following RSV infection during pregnancy, but small-scale studies have not identified any significant associations.[111]

A number of vaccines against RSV, using various platforms, are under clinical investigation. The only RSV vaccine currently approved for use in pregnant women (May 2023) is an unadjuvanted bivalent (RSV-A and RSV-B subtype) subunit prefusion protein vaccine (ABRYSVO, Pfizer, New York, NY).

Maternal Respiratory Syncytial Virus Vaccine

Safety

A systematic review on the safety of RSV vaccination, including six RCTs involving 17,991 pregnant women (four studies of RSV pre-F protein vaccines and two of a RSV F protein nanoparticle vaccine)[112] showed no significant association between maternal RSV vaccination and intrauterine growth restriction (RR: 1.32, 95% CI: 0.75–2.33), stillbirth (RR: 0.81, 95% CI: 0.38–1.72), maternal death (RR: 3.00, 95% CI: 0.12–73.50), congenital abnormalities (RR: 0.96, 95% CI: 0.88–1.04), or infant deaths (RR: 0.81, 95% CI: 0.36–1.81).[112] The risk of maternal RSV vaccine predisposing to preterm birth is uncertain (RR: 1.16, 95% CI: 0.99–1.36), with a signal emerging from two studies.[113] [114] The clinical development of the RSV prefusion F protein vaccine produced by GlaxoSmithKline was terminated after a higher rate of preterm births (RR: 1.37; 95% CI: 1.08–1.74) was found in vaccine recipients (6.8%) compared with placebo (4.9%).[114] For the Pfizer RSV bivalent pre-F protein (MATISSE trial), although adverse events were not statistically different between the vaccine and placebo groups, the preterm birth rate was 5.6% in the vaccine group and 4.7% in the placebo group (RR: 1.20; 95% CI: 0.98–1.46). A post hoc analysis showed preterm birth rates were higher in UMICs (7.4 vs. 4.0%), but similar in HICs (5.0 vs. 5.1%), LMICs (3.1 vs. 5.9%), and low-income countries (2.6 vs. 2.5%). Notably, preterm births mostly occurred at 35 to 36 weeks of gestation births and were not linked to timing of vaccination and occurred during the SARS-CoV-2 delta variant period.[115] This signal of an increase in preterm births led to licensure in of the Pfizer ABRYSVO vaccine in the United States to be administered to pregnant women between 32- and 36-weeks of gestational age. To date, postlicensure safety surveillance in the United States shows no increase in preterm birth rates.[116]

Immunogenicity

Immunogenicity from four RCTs analyzed in a systematic review observed significant increases in RSV neutralizing antibodies (Nab; Nab-A, Nab-B, and anti-RSV F protein-specific IgG; F-IgG), following vaccination in both maternal and infant cord blood sera.[117] In mothers, the geometric antibody titers at delivery showed a pooled standard mean difference (SMD) for Nab-A of 4.14 (95% CI: 2.91–5.37), Nab-B of 3.95 (95% CI: 2.79–5.11), and F-IgG of 12.20 (95% CI: 7.76–16.64).

Similarly, significantly higher antibody titers of all types were found in infants born to vaccinated mothers compared with control groups. Antibody levels in infants at birth showed pooled SMDs for Nab-A of 3.9 (95% CI: 2.81–4.99), Nab-B of 1.86 (95% CI: 1.09–2.62), and F-IgG of 2.24 (95% CI: 1.24–3.23).

Efficacy and Effectiveness

The landmark phase-III observer–blind placebo-controlled maternal RSV vaccine trial of a recombinant RSV fusion (F) protein nanoparticle vaccine (PREPARE trial) demonstrated the first proof-of-concept for the efficacy of maternal RSV vaccination against medically significant symptomatic RSV LRTI in infants.[118] The PREPARE study enrolled 4,636 healthy pregnant women between 28 and 36 weeks' gestational age at 87 sites across 11 countries. Despite the vaccine being safe and immunogenic, the study failed to reach the primary endpoint and reported a VE of 39.4% (95% CI: −1.0 to 63.7) against medically significant RSV-LRTI through 90 days of life. The VE was 44.4% (95% CI: 19.6–61.5%) against hospitalization for infant RSV-LRTI, and 48.3% (95% CI: −8.2 to 75.3) against RSV-LRTI with severe hypoxemia. Importantly, this study demonstrated an effect on all-cause LRTI, with vaccine efficacies of 23.2% (95% CI: 1.4–40.2), 27.8% (95% CI: 4.8–45.3), and 46% (95% CI: 21.8–64.2) for all-cause medically significant LRTI, hospitalization rates, and severe hypoxemia, respectively.

The MATISSE trial was a phase-III double-blind, placebo-controlled trial, evaluated across 18 countries in pregnant women between 24 and 36 weeks' gestation, which showed that the VE against severe, medically attended RSV LRTIs in infants was 81.8% (95% CI: 40.6–96.3) at 90 days, and 69.4% (95% CI: 44.3–84.1) at 180 days after birth.[115] Vaccine effectiveness studies are yet to be published.

Other Considerations

With the implementation of maternal RSV vaccination, the need to address potential interactions with currently administered vaccines is paramount. Recent studies exploring the effect of coadministration of RSV and Tdap vaccines have shown interference of immune responses.[119] [120] Participants receiving the RSVPreF3 had lower immune responses of all components of Tdap, most notable with pertussis antigens. Contrastingly, a phase II RCT exploring an RSV fusion protein vaccine (RSVPreF3) coadministered with Tdap demonstrated no interference of Tdap with response to RSVPreF3 immunogenicity.[119] Levels of RSV-A neutralizing antibody increased ≥8-fold and anti-RSVPreF3 IgG antibody ≥11-fold at 1-month postvaccination, persisting for up to 12 to 18 months.[119] Similarly, coadministration of ABRYSVO (RSVpreF) with Tdap showed noninferiority criteria were not met for pertussis humoral immune responses.[120] While interference of diphtheria and tetanus antigens were not shown to have clinical relevance, the absence of an established seroprotective threshold for pertussis makes this conclusion difficult to draw in this case. Other studies have also shown reduced immune responses to influenza vaccine when coadministered with RSVpreF. However, further research into the mechanisms and clinical relevance is required.[121]

Severe Acute Respiratory Syndrome Coronavirus-2 Vaccine

In late 2019, the first cases of a distinct viral pneumonia were detected in the Wuhan region of China, spreading rapidly throughout the globe, officially declared a pandemic in March 2020 by the WHO.

Several observational studies published at the beginning of the pandemic and later corroborated by epidemiological systematic analyses reported that pregnant women were at an increased risk of severe COVID-19 disease.[21] [122] Although this risk was lower during the era when the Omicron variant circulated compared with the pre-Omicron era, pregnant women remained at a higher risk of hospital and intensive care unit (ICU) admission, mechanical ventilation, and death.[21] [123] [124] [125] In comparison with nonpregnant women of similar age, pregnant women hospitalized for COVID-19 were more likely to require admission to the ICU (OR: 2.61, 95% CI: 1.84–3.71) and to be mechanically ventilated (2.41, 95% CI: 2.13–2.7). Further, COVID-19 was associated with a 6-fold (6.09, 95% CI: 1.82–20.38) higher risk of death in pregnant women compared with the nonpregnant general population.

Pregnant women with COVID-19 also had higher risks of adverse pregnancy and birth outcomes. Notably, the odds of hypertensive disorders were significantly increased in pregnant women that had COVID-19, including preeclampsia (OR: 1.62; 95% CI: 1.45–1.82), severe preeclampsia (OR: 1.76; 95% CI: 1.18–2.63), eclampsia (OR: 1.97; 95% CI: 1.01–3.84), and HELLP syndrome (OR: 2.10; 95% CI: 1.48–2.97).[126] Adverse fetal and neonatal outcomes included an increased risk of stillbirths (aOR: 2.21, 95% CI: 1.58–3.11), preterm birth (OR: 1.57, 95% CI: 1.36–1.81), and neonatal ICU admissions (2.18, 95% CI: 1.46–3.26) in pregnant women with COVID-19 compared with those without.[21] [127]

Severe COVID-19 in infants under 6 months of age was low compared with other high-risk groups, and the incidence was reported as higher in children 6 months and 5 years.[128] There are presently no COVID-19 vaccines licensed for use in infants less than 6 months and the protection of young infants against COVID-19 would depend on vaccination of pregnant women to enhance transplacental transfer of protective antibodies to the fetus.

During the COVID-19 pandemic, 10 COVID-19 vaccines received an Emergency Use Listing from the WHO, some of which have since gone on to be fully licensed for use including for pregnant women.[129] Platforms being utilized include mRNA (Pfizer/BioNTech; Moderna), protein subunit (Novavax), nonreplicating viral vector (Oxford-AstraZeneca; Janssen; Sputnik V), and inactivated whole virus (Sinovac; Sinopharm; Valneva; Bharat Biotech) vaccines.

Maternal COVID-19 Vaccine

Safety

Early clinical trials using mRNA vaccines in healthy adults showed high VE (∼95%) to the circulating viral strain at the time and were classified as having good safety profiles.[130] [131] Although pregnant women were excluded from initial clinical trials, incidental pregnancies were noted during preauthorization trials, with no adverse outcomes recorded in these.[131] [132] [133] [134] [135] The use of mRNA vaccines increased in pregnant women following FDA approval of the Pfizer/BioNtech mRNA vaccine and the Moderna mRNA vaccine for Emergency use authorization (EUA) in April 2021. This approval was guided by preliminary evidence from both active (V-Safe Surveillance and pregnancy Registry) and passive (the Vaccine Adverse Events Reporting System, VAERS) surveillance systems demonstrating safety in pregnant women.[136] Postmarketing surveillance and observational studies have also found good safety profiles of other commonly used vaccine platforms, including viral vector and inactivated vaccines.[137]

Vaccine safety monitoring systems, such as the U.S.-based VAERS, v-safe, the v-safe COVID-19 Vaccine Pregnancy Registry, and the Vaccine Safety Datalink, as well as the European Medicines Agency (EMA) continue to amass evidence that COVID-19 mRNA vaccines administered during pregnancy are safe for both mother and infant.[136] [137] [138] [139] Similar side effect profiles were noted among pregnant and nonpregnant vaccine recipients. Side effects were mild or moderate and generally self-limiting.[129] There is currently no evidence that vaccination increases the risk of miscarriages, premature birth, low birth weight, neonatal encephalopathy, fetal death, or fetal abnormalities.[139] [140]

Immunogenicity

mRNA vaccination in pregnant women leads to robust antibody levels and efficient transplacental transfer of anti-SARS-CoV-2 IgG to the fetus,[141] [142] [143] [144] while neutralizing antibodies in neonates born to women vaccinated with COVID-19 have been shown to persist up to at least 12 weeks of age.[144]

Efficacy and Effectiveness

Following extensive real-world use, mRNA COVID-19 vaccines were found to be effective for both mother and infant.[137] Single doses of vaccines administered during pregnancy, in any trimester, was associated with 54% reduction in SARS-CoV-2 infection (OR: 0.46, 95% CI: 0.28–0.76) and 59% reduction in COVID-19-related hospitalizations (OR: 0.41, 95% CI: 0.33–0.51) in pregnant women. Following a second dose of vaccine, during the course of the COVID-19 pandemic, greater reductions were observed against SARS-CoV-2 infection (OR: 0.31, 95% CI: 0.16–0.59), and COVID-19-related hospitalization (OR: 0.15, 95% CI: 0.10–0.21). However, current widespread immunity, following prior infection or vaccination, necessitates the use of only a single “booster” dose of vaccine in pregnancy, in contrast to protocols during the pandemic when both primer and booster vaccine doses were needed in a largely SARS-CoV-2 naïve population.

In infants younger than 6 months of age, using a case–control test-negative study design, the effectiveness of maternal vaccination during pregnancy was 52% (95% CI: 33–65) against COVID-19 hospitalization in infants born to women who were vaccinated against COVID-19 with two mRNA vaccines (either BNT162b2, Pfizer–BioNTech or mRNA-1273, Moderna).[145] Higher effectiveness was observed during the delta variant period (80%; 95% CI: 60–90) compared with the Omicron period (38%; 95% CI: 8–58), in studies where the index-virus (wild-type SARS-CoV-2) vaccine constructs were being used. It was postulated that the lower effectiveness in the Omicron period was most likely due to a mismatch of vaccine and circulating virus variants. In addition, higher effectiveness was noted among mothers who were vaccinated after 20 weeks of pregnancy (69%; 95% CI: 50–80) compared with those vaccinated in the first 20 weeks (38%; 95% CI: 3–60) of pregnancy. Notably, much of the data were based on index-virus vaccine, rather than subsequent updated vaccines.[146]

Considerations for Maternal Vaccination Implementation

There are a number of factors that result in low vaccine uptake among pregnant women globally.[147] Recent estimates from the United States showed that 61% of pregnant women received seasonal influenza vaccines, whereas just over half (56%) received aP-containing vaccines.[148] Geographical and sociodemographic disparities can result in significantly lower coverage rates, with some LMICs reporting influenza vaccination in less than 16% of the pregnant population.[149] Reducing morbidity and mortality, particularly in LMICs where the burden is greatest, requires a concerted effort to reduce vaccine hesitancy, enhance vaccine delivery platforms, and nurture effective stakeholder engagement.

Addressing Vaccine Hesitancy

Despite strong recommendations by various agencies including the WHO, CDC, and EMA, globally, vaccine hesitancy remains high.[147] [150] Several strategies to instill confidence in mothers and increase vaccine uptake can be undertaken. Educational campaigns help to promulgate the benefits and safety of maternal immunization and should be coupled with commensurate healthcare provider training to effectively discuss the importance of vaccination and address common concerns or fears.[151] [152] Broader communication engagement initiatives can be used to foster buy-in from community leaders and social influencers to advocate for vaccination and address community concerns, as well as debunking vaccine misinformation and disinformation.[153] Further, community engagement can inform ethnographically appropriate communication content and strategies.[154]

Improving Delivery and Administration Pathways

Accessibility and convenience are essential to promote maternal vaccine uptake.[155] Vaccinations should be readily available at clinics, community health centres, and through outreach initiatives such as mobile clinics or home visits.[156] Regular reminders, prompts, and follow-ups can be used through postal services, door-to-door visits and, where available, eHealth communication strategies.[157] Vaccines should either be provided free of charge, covered by health insurance, or provided at low cost to reduce financial burdens.[158]

In most settings, maternal vaccines are delivered through antenatal platforms. The WHO currently recommends a minimum of eight contacts recommended to reduce perinatal mortality and improve women's experience of care during pregnancy.[159] Therefore, considerations for vaccination during pregnancy should take into account the frequency of antenatal visits, seasonality of circulating viruses and appropriate timing of vaccination to maximize protection of both mother and infant. Time frames for administration of recommended vaccines, and coadministration are depicted in [Fig. 2]. Coadministration during a single visit may be necessary in settings where pregnant women struggle to attend the recommended antenatal contacts or present late in pregnancy for antenatal care.[160] Evidence-based guidelines for safe and effective coadministration of vaccines should be made available to health care practitioners with integrated monitoring, communication, and feedback mechanisms. The CDC recommends the coadministration of COVID-19, influenza, and RSV vaccines; however, as described above, reduced immunogenicity to pertussis and influenza antigens with coadministration with the RSV vaccine have been described. Further research into the clinical outcomes of vaccine coadministrative practices are warranted.

Engaging all Stakeholders

Local and international policymakers are vital to the development and implementation of policies and protocols that prioritize maternal vaccination as part of standard antenatal care. Additionally, policies for the sustained fiscal investment in strengthening health care infrastructure would improve both accessibility to vaccines and convenience thereof, as well as delivery pathways of maternal vaccination, including logistics and workforce capacity.[155] [165] Cost-effectiveness and cost–benefit analyses advocating for the implementation of maternal vaccination strategies are crucial to policymakers. These could include demonstrating reduction in hospitalization and health system burden, prevention of severe disease, and long-term health benefits (such as the reduction of long-term respiratory disease and financial burden on families).[166]

Engagement with the pharmaceutical industry from governmental bodies and nongovernmental organizations can be leveraged to ensure vaccine supply and availability, promote ongoing research and development, and ensure affordability, particularly for LMIC's, through vertical pricing models, donations or collaboration with international health organizations.[147] [167] Global organizations such as the Global Alliance for Vaccines Initiative (GAVI) can foster equitable access to vaccines around the world, with financial support, cost-negotiation, technical assistance, and training.[168]

Conclusion

LRTIs are a common cause of morbidity and mortality in children under the age of 5 years, with a significant proportion of the burden concentrated in early infancy. For many common respiratory pathogens, infant and childhood vaccines are available but ineffective at providing protection during the vulnerable newborn period. To overcome this burden, maternal vaccination offers an effective and achievable strategy in reducing the burden of LRTI in both mothers and their offspring. Vaccines with demonstrated safety and effectiveness profiles currently recommended in pregnancy include those against pertussis, influenza, COVID-19, and RSV. Future investment in broadening the scope of maternal vaccines as well as their effective rollout and coverage is essential to reduce the burden in infancy, particularly in LMICs.

Conflict of Interest

None declared.

^* Joint senior author

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Article published online:
21 December 2024

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