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Vaccine 33 (2015) 64366440

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Maternal benets of immunization during pregnancy

Geeta K. Swamy a, , Richard H. Beigi b
Department of Obstetrics and Gynecology, Duke University, Durham, NC, United States
Department of Obstetrics, Gynecology and Reproductive Sciences, Magee-Womens Hospital of the University of Pittsburgh Medical Center,
Pittsburgh, PA, United States

a r t i c l e i n f o a b s t r a c t

Article history: The US Centers for Disease Control & Prevention currently recommend routine immunization to prevent
Available online 16 September 2015 17 vaccine-preventable diseases that occur in infants, children, adolescents, or adults. Pregnant women
are at particularly high risk for morbidity and mortality related to several vaccine-preventable diseases.
Keywords: Furthermore, such illnesses are also associated with adverse pregnancy outcomes such as spontaneous
Maternal immunization abortion, congenital anomalies, preterm birth, and low birthweight. In addition to directly preventing
maternal infection, vaccination during pregnancy may offer fetal and infant benet through passive
Passive immunity
immunization. Several vaccines aimed at providing passive immunity to neonates are either currently
recommended or in development. This article specically addresses maternal benets of maternal immu-
nization following (1) vaccines recommended for all pregnant women; (2) vaccines recommended for
pregnant women with particular risk factors; and (3) novel vaccines currently under development that
primarily aim to at reduce infant morbidity and mortality.
2015 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY license

1. Introduction pregnancy [4]. In addition to the six vaccines (vaccines against

inuenza, Tdap, pneumococcus, meningococcus, Hepatitis A and
Pregnancy is a particularly susceptible period for maternal and B) that are currently recommended by the US Centers for Dis-
infant complications associated with vaccine preventable diseases ease Control & Prevention (CDC) for use during pregnancy (with
(VPDs). Pregnant women are at high risk for inuenza-related some contingent upon risk factors), novel vaccines against group B
morbidity and mortality, including higher rates of hospitalization, streptococcus and respiratory syncytial virus are currently being
cardiopulmonary complications, and death compared to the gen- evaluated for administration during pregnancy [57]. Although
eral public [1]. Maternal inuenza infection is associated with novel vaccine candidates are focusing primarily on the potential
adverse birth outcomes including preterm birth, fetal growth for infant disease prevention, this article specically addresses
restriction, and fetal demise [1]. Both maternal and fetal compli- maternal benets of immunization during pregnancy following:
cations are further elevated during pandemic inuenza seasons. (1) vaccines recommended for all pregnant women; (2) vaccines
Maternalfetal transmission of varicella and rubella are associated recommended for pregnant women with particular risk factors;
with congenital malformations and life-long infection in the case of and (3) vaccines primarily aimed at reducing infant morbidity and
hepatitis B. Beyond preventing maternal and fetal infection, mater- mortality (Table 1).
nal immunization should provide infant protection through passive
immunization, i.e. via transplacental transfer of maternal IgG anti-
bodies as well as transfer of maternal IgA antibodies via breast 2. Vaccines recommended for all pregnant Women
milk [2,3]. The potential for passive immunization to protect young
infants against pertussis infection has been the primary driver for 2.1. Inuenza
the recent recommendation for administration of tetanus, diphthe-
ria, acellular pertussis (Tdap) vaccination during each and every Approximately 20% of the US population will have inuenza dur-
ing a single non-pandemic season compared to nearly 50% during a
pandemic season [1]. Similarly, 20% of pregnant women will suffer
from an inuenza-like illness (ILI) during a non-pandemic season,
Corresponding author at: Duke University, 2608 Erwin Rd, Suite 210 Durham, with 10% having laboratory-conrmed inuenza [8]. Presumably
NC 27705, United States. Tel.: +1 919 668 1600; fax: +1 919 613 1550. due to changes in immunology and cardiorespiratory physiology
E-mail address: (G.K. Swamy). rather than susceptibility to acquisition, pregnant and immediately
0264-410X/ 2015 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY license (
G.K. Swamy, R.H. Beigi / Vaccine 33 (2015) 64366440 6437

Table 1
Licensed and novel vaccines for pregnant women.

Vaccines recommended for all pregnant Vaccines recommended for pregnant women with risk factors Novel vaccines aimed at reducing infant infection
women through maternal immunization

Inactivated inuenza vaccine (IIV) Pneumococcal polysaccharide 23-serotype vaccine (PPSV23) Trivalent group B streptococcus polysaccharide
Tetanus, diphtheria, acellular pertussis (Tdap) Meninogococcal tetravalent polysaccharide vaccine (MPSV4) Inactivated respiratory syncytial virus vaccine
Inactivated hepatitis A vaccine
Recombinant hepatitis B vaccine

postpartum women are at high risk for inuenza-related morbidity 2.2. Tetanus, diphtheria, and pertussis
and mortality including hospitalization, cardiopulmonary compli-
cations, and death [9]. Beyond maternal complications, inuenza Childhood vaccination combined with decennial booster and
infection in pregnancy is associated with adverse birth outcomes exposure-related dosing against tetanus and diphtheria has led to
including spontaneous abortion, preterm birth, low birthweight, the near eradication of both diseases in the US. Pertussis or whoop-
and fetal demise [1]. Both maternal and fetal complications increase ing cough, however, has been on the rise for the last two to three
even further during pandemic seasons [10,11]. decades following a long period of active disease control and pre-
Based on the potential for maternal morbidity and mortal- vention. Although the incidence of pertussis has increased across
ity associated with inuenza during pregnancy, the CDC and the entire population, disease-related morbidity and mortality pri-
the American College of Obstetrics & Gynecology (ACOG) recom- marily affects infants [19]. Infants are most commonly exposed to
mend inactivated inuenza vaccine (IIV) for all women who will pertussis through close contact, with 4760% of cases due to expo-
be pregnant during inuenza season [12]. Initial recommenda- sure from infected parents [20]. Furthermore, adults with pertussis
tions for IIV administration during pregnancy made in 1997 were are often unaware of their diagnosis, given that many adults are
extrapolated from the documented efcacy and safety of IIV in non- either asymptomatic or have symptoms of a common cold.
pregnant adults. Until the 2009 pandemic, there were only a few Vaccination efforts to reduce the incidence of pertussis among
small-scale studies on the safety and immunogenicity of mater- young infants have previously focused on cocooning, or strate-
nal inuenza vaccination. In a randomized trial of 340 pregnant gies to immunize close contacts of young infants against pertussis.
women in Bangladesh, Zaman et al. demonstrated a 36% reduction The initial strategy including immediate postpartum maternal
in laboratory-conrmed inuenza among women who received IIV vaccination combined with antenatal vaccination among previ-
during the third trimester compared to women who received pneu- ously non-vaccinated pregnant women failed to affect the ongoing
mococcal vaccine [2]. While this study was potentially limited by pertussis outbreaks. In October 2012, the CDC changed its rec-
the lack of a placebo control group, Madhi et al. recently com- ommendation on vaccination during pregnancy, now advising
pleted a randomized trial of IIV vs. placebo in 2000 pregnant obstetric providers to administer Tdap during each pregnancy,
women in South Africa [13]. With inuenza attack rates of 3.6% vs. regardless of prior Tdap receipt [4]. This strategy is based on
1.8% among HIV uninfected placebo and IIV groups respectively, the concept of passive immunization in which maternally-derived
IIV vaccine efcacy in this pregnant population was 50.4% (95% vaccine-induced antibodies cross the placenta into the fetal cir-
CI 14.571.2). For women with HIV infection, vaccine efcacy was culation. Passive immunization can protect young infants during
57.7% (95% CI 0.282.1) with attack rates of 17% vs. 7% for placebo the rst few months of life when they are most vulnerable to per-
and IIV groups, respectively. Black et al. were unable to demonstrate tussis and prior to establishing immunity from their own primary
vaccine effectiveness against hospital admissions and physician vaccination series [20,21].
outpatient visits due to respiratory illness among pregnant women While it is imperative that we continue efforts to reduce the
cared for in a health system level analysis over ve consecutive incidence of infant pertussis, many questions remain regarding
non-pandemic seasons [14]. The lack of demonstrated effectiveness the potential benets and/or risks of Tdap administration during
may be due to the use of respiratory illness rather than laboratory pregnancy, including the potential effect of repeated close-interval
conrmed inuenza and that hospitalizations among the entire dosing among women having more than one pregnancy in a rel-
population of pregnant women were uncommon, regardless of atively short period of time, e.g. 13 years, and whether repeated
vaccination status. However, a population-based study of 117,347 doses of Tdap actually continues to boost pertussis antibody levels
Norwegian women who were pregnant during the 20092010 pan- in pregnant women. Although relatively small with 48 pregnant
demic revealed a 70% reduction in clinical diagnosis of inuenza, and 32 non-pregnant, Tdap nave women, Munoz et al. demon-
suggesting that vaccine efcacy during a novel pandemic season strated that Tdap administration during pregnancy is immunogenic
may offer even greater maternal benet than seasonal vaccination and safe [22]. However, the overall lack of data on the potential
[15]. maternal benet of Tdap vaccination, i.e., to prevent pertussis in
Successful public health promotion by the CDC and ACOG led pregnant women themselves, as well as the lack of both immuno-
to inuenza vaccine coverage exceeding 50% for the rst time genicity and safety data following repeated Tdap administration,
in 20122013 [16]. Studies assessing vaccine acceptance have represents a signicant knowledge gap. Ongoing larger-scale stud-
clearly identied a lack of knowledge of recommendations, lack ies of Tdap during pregnancy will provide much needed data in the
of obstetric provider recommendation, and lack or misunderstand- near future [23,24].
ing of safety data during pregnancy as the key factors inuencing
inuenza vaccine uptake during pregnancy [17,18]. Thus, con- 3. Vaccines recommended for all pregnant women with
tinued research on inuenza vaccination during pregnancy and risk factors
education of obstetric providers and pregnant women is warranted.
With approximately 4 million births in the US annually, maternal 3.1. Pneumococcal disease
inuenza immunization has great potential to improve maternal
health during pregnancy and the immediate postpartum period Pneumococcal disease, caused by the Gram-positive Strep-
when the risks of inuenza are greatest. tococcus pneumoniae bacterium, is associated with substantial
6438 G.K. Swamy, R.H. Beigi / Vaccine 33 (2015) 64366440

morbidity and mortality resulting from pneumonia, bacteremia, for use during pregnancy based on risk factors described
and meningitis [25]. Pneumococcal pneumonia, the most common above [29].
manifestation, affects 900,000 Americans and results in 400,000
hospitalizations and 57% mortality each year. Less common pre-
sentations include bacteremia and meningitis, which affect about 3.3. Hepatitis A
12,000 and 3000 individuals each year, respectively, with 1015%
mortality. Although the incidence of pneumonia during pregnancy Although generally self-limiting, hepatitis A virus (HAV) causes
is fairly low, the disease course is similar to that of inuenza, likely fever, vomiting, and jaundice due to acute liver infection. As HAV
attributable to the same pregnancy-associated physiologic respira- is transmitted via fecal-oral contamination from close contact with
tory changes and alterations in cell-mediated immunity, resulting infected individuals or contaminated food or drinks, the general
in higher rates of hospitalization, acute respiratory distress syn- public is at risk for HAV infection [34]. Widespread vaccination
drome (ARDS), cardiorespiratory failure, and death [26]. Obstetric against HAV in the US began in 1999 and has led to a signi-
complications include fetal distress, preterm birth, and low birth- cant drop in documented cases of HAV in the US [35]. Although
weight [26]. HAV vaccination is currently included in the CDC recommended
Current CDC guidelines recommend the 23-serotype polysac- childhood immunization schedule, vaccination against HAV is also
charide vaccine (PPSV23) for children and adults with chronic recommended for people with high risk for HAV exposure: those
medical conditions and other risk factors including chronic heart traveling to endemic areas, men who have sex with men, those
or lung disease (asthma, diabetes, cigarette smoking), alco- in close contact with individuals with HAV infection or receipt
holism, chronic liver disease, cerebrospinal uid leaks, cochlear of clotting-factor concentrates, and laboratory or healthcare staff
implants, congenital or acquired immunodeciencies, diseases working with biological specimens. Consistent with CDC guide-
requiring immunosuppressant therapy, sickle cell disease and lines, pregnant women with identiable risk factors should receive
other hemoglobinopathies, and functional or anatomic asplenia HAV vaccine [34]. Although the data on HAV vaccine safety during
[27]. In addition, the 13-serotype pneumococcal conjugate vaccine pregnancy is lacking, the current inactivated HAV vaccine does not
(PCV13) is recommended for all children and additional high risk contain live virus components and is exceedingly unlikely to carry
adult subpopulations [28]. While currently available data do not any risk of maternal or fetal harm.
support the need for widespread use of PCV13 or PPSV23 during
pregnancy [29], a systematic review of observational studies and a 3.4. Hepatitis B
randomized trial of PPSV23 given during pregnancy demonstrated
no maternal or fetal safety concerns [22,30]. Furthermore, maternal Associated with acute liver inammation, vomiting, and jaun-
PPSV23 vaccination provides protective antibody levels for at least dice, hepatitis B virus (HBV) can either be self-limiting or lead to
one year following delivery and higher neonatal antibody levels. A a chronic carrier state with long-term morbidity (cirrhosis, liver
recent Cochrane review found insufcient evidence to suggest that cancer, liver failure) and mortality. Individuals with close contact
maternal vaccination could reduce infant pneumococcal infection with an HBV-infected individuals blood and bodily uids are at risk
via passive immunization [31]. Nevertheless, in accordance with for disease. The three-dose recombinant DNA HBV vaccine series
CDC guidelines for adult immunization, PPSV23 should be given to provides indenite immunity in most individuals (>90%) and is
pregnant women for their own benet with additional risk factors currently initiated at birth as part of the CDC recommended child-
as described above. hood immunization schedule [36]. Vaccination against HBV has
been proven to be effective given the greater than 60% reduction in
reported cases of HBV over the last 1520 years [35].
3.2. Meningococcal disease Much of the attention on HBV during pregnancy focuses on
the risk of perinatal transmission following primary or chronic
Neisseria meningitidis causes rare, but often deadly, meningi- maternal infection, particularly given the high risk of chronic dis-
tis and sepsis in about 1000 people in the US each year [32]. ease development following perinatal acquisition. As part of that
Although susceptible to antibiotics, meningococcal disease carries focus, pregnant women are routinely screened for HBV via surface
a mortality rate of 1015% and a 20% rate of severe morbidity antigen (HBsAg) testing followed by neonatal treatment with HB
among survivors including limb amputations, strokes, and neu- immunoglobulin (HBIg) prophylaxis and HBV vaccination during
rocognitive abnormalities. In 2005, the tetravalent meningococcal the rst hours of life for infants born to HBV infected mothers [37].
conjugate vaccine (MCV4) was included in the US adolescent vacci- However, unvaccinated pregnant women with risk factors for HBV
nation schedule, replacing the tetravalent polysaccharide vaccine acquisition should be counseled on the extremely high effective-
(MPSV4) based on a longer duration of vaccine-induced immu- ness of HBV vaccination to prevent maternal and subsequent fetal
nity with MCV4. Similar to PPSV23 and PCV13, there are several infection. Individuals at high risk of HBV acquisition include those
adult subgroups who are at high risk for meningococcal infection: with one or more sexual partner in the past six months, household
those in close living conditions such as dormitories or military bar- or sexual contact with an HBV-infected individual, or intravenous
racks, those with complement deciencies, functional or anatomic drug use [36]. Although extensive safety data are limited, HBV
asplenia, those residing in hyperendemic areas, and laboratory staff vaccination during pregnancy has not been associated with any
working with N. meningitidis. maternal or fetal complications [30]. Therefore, the three-dose HBV
Previously unvaccinated pregnant women with risk factors vaccine series should be initiated for previously unvaccinated or
for meningococcal disease should be vaccinated. Although MCV4 incompletely vaccinated pregnant women with risk factors for HBV
and MPSV4 are both inactivated products which should not infection.
carry any maternal or fetal risk, available data on meningococ-
cal vaccination in pregnancy involves MPSV4 rather than MCV4.
A systematic review of maternal MPSV4 demonstrated no con- 4. Novel vaccines aimed at reducing infant infection
cern for maternal or fetal complications [30]. ODempsey et al. through maternal immunization
demonstrated an adequate maternal antibody response follow-
ing MPSV4 vaccination in the third trimester [33]. Given the Similar to the recommendation for Tdap to be administered dur-
lack of available safety data on MCV4, MPSV4 is recommended ing pregnancy, additional vaccines focused on prevention of group
G.K. Swamy, R.H. Beigi / Vaccine 33 (2015) 64366440 6439

B streptococcus (GBS) and respiratory syncytial virus (RSV) during symptomatic individuals, 16% required hospitalization with 4%
early infancy are in development. mortality and disease burden estimates similar to inuenza [47].
We recently published a series of three cases of RSV infection during
4.1. Group B Streptococcus pregnancy, two of which required maternal mechanical ventila-
tion and critical care due to severe respiratory compromise [48].
GBS is leading cause of invasive infection within the rst three Given the similarities with inuenza, it is very possible that the
months of life, resulting most commonly in sepsis and meningitis incidence and associated complications of maternal RSV infection
[38]. Intrapartum antibiotic prophylaxis has signicantly reduced have been underestimated. If this is in fact the case, the potential
the incidence of early-onset neonatal GBS (within the rst seven for a combined maternal and infant benet of an efcacious RSV
days of life) in the US. However, there has been no change in vaccine could be great.
the rates of late-onset GBS disease (from one week to three
months of age), which occurs in 0.290.47 per 1000 live births and 5. Summary
can be equally devastating. Furthermore, strategies of screening
plus intrapartum antibiotic prophylaxis are often impractical in Pregnant women have unique and heightened susceptibilities
low-resources settings. Based on available evidence of neonatal to greater morbidity and mortality from a variety of bacterial
protection against GBS disease in the setting of passive immu- and viral vaccine-preventable diseases. Currently signicant atten-
nity [39], a vaccine against GBS could have a signicant impact on tion is focused on developing vaccines for use during pregnancy
preventing both early- and late-onset disease. with the primary goal of preventing infections in young infants.
Albeit the primary objective of a GBS vaccine will be to While this approach holds tremendous potential for sizable disease
reduce infant infection, it is highly plausible that a GBS vaccine prevention in infants, pregnant women also have signicant oppor-
would have signicant benets for maternal health and ultimately tunity for disease prevention from both currently recommended
overall pregnancy outcomes. In addition to asymptomatic cervico- and future vaccines. Maternal-child health can and will continue to
vaginal colonization, GBS causes numerous maternal infections be improved with ongoing efforts to prevent numerous infectious
[40]. Although most GBS urinary tract infections are asymptomatic, diseases in both mothers and infants.
GBS causes about 10% of acute pyelonephritis in pregnancy, which
is highly concerning given the association of pyelonephritis with
Conict of interest
adverse pregnancy outcomes (preterm birth, low birthweight, fetal
demise) [41]. Intra-amniotic infection (IAI) is caused by the ascend-
The authors declare no conicts of interest to report.
ing spread of vaginal ora, with GBS detected in the amniotic uid
of 15% of cases. Maternal consequences of IAI include serious mater-
nal pelvic infections, sepsis, and postpartum hemorrhage. Maternal Funding
bacteremia occurs in 26% of IAI cases overall and in up to 35%
of cases with conrmed GBS-related puerperal infection IAI and Dr. Swamy has received support from GlaxoSmithKline Inc.,
postpartum endometritis. While septic shock is rare, GBS sepsis Novartis Vaccine Inc., and Novavax to conduct research funding
follows bacteremia in 525% of cases [42]. for clinical trials in immunization. Dr. Beigi has received research
A trivalent conjugated GBS vaccine is being evaluated in phase II funding for clinical trials in immunization from Novartis Vaccines
and III studies in pregnant women, with a focus on third trimester Inc., Novavax, and Genocea BioSciences.
administration to theoretically maximize passive immunity at the
height of antibody transfer rates [6,43]. Although the morbidity References
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