HUMAN VACCINES & IMMUNOTHERAPEUTICS 2016, VOL. 12, NO. 4, 894–902 http://dx.doi.org/10.1080/21645515.2015.1132129

REVIEW

Viral hepatitis vaccination during pregnancy Yueyuan Zhaoa, Hui Jina,b, Xuefeng Zhangc, Bei Wanga,b, and Pei Liua a School of Public Health, Southeast University, Nanjing, China; bKey Laboratory of Environmental Medicine Engineering, Ministry of Education, Nanjing, China; cJiangsu Provincial Center for Disease Control and Prevention, Nanjing, China

ABSTRACT

ARTICLE HISTORY

Viral hepatitis is a serious global public health problem. It is also a common cause of jaundice and gestational complications in pregnant women. Moreover, infected mothers can transmit the virus to their fetus or neonate, which may increase disease burden and decrease quality of life. To date, commercial vaccines have been developed for hepatitis A, B, and E and are available to the general population. The Advisory Committee on Immunization Practices currently accepts emergency vaccination against hepatitis A and B during pregnancy due to benefits that overweight the potential risks. While there are limited data from trials with limited numbers of samples that suggest the efficacy or safety of hepatitis B and E vaccines in pregnant women, additional data are necessary to provide evidence of vaccination during pregnancy.

Received 31 August 2015 Revised 27 November 2015 Accepted 11 December 2015

Introduction Viral hepatitis, mainly caused by the hepatitis A, B, C, D, and E viruses, is an inflammation of the liver and an important global health challenge. More than 400 million people are estimated to be infected worldwide, and 1.4 million die annually from viral hepatitis.1,2 Viral hepatitis also causes liver disease during pregnancy, prevention and control of mother-to-child transmission is an important issue for pregnant population. Vaccination can effectively prevent horizontal and vertical transmission of hepatitis B or C, which directly decreases the global burden of this disease.3 While the inactive vaccines administered to pregnant women are theoretically believed to not increase the risk of adverse outcomes for mothers or fetuses,4-6 the Advisory Committee on Immunization Practices (ACIP) currently accepts administration of only 2 vaccines (influenza and Tdap [tetanus, diphtheria, and pertussis]) during pregnancy.7 The administration of other vaccines to pregnant women should be based on whether the benefits outweigh the risks.8 Viral hepatitis vaccination during pregnancy benefits not only the mothers but also developing fetuses owing to passive protection from the mother.3 Therefore, vaccination of susceptible or high-risk pregnant women should be considered.9,10 The current study reviews data on viral hepatitis vaccination during pregnancy.

Hepatitis A Hepatitis A virus (HAV) infection is a leading cause of acute hepatitis worldwide. However, this infection is associated with fewer than 2% of hepatitis cases in pregnant women,11-13 with fewer than 1/1,000 pregnant women infected with acute hepatitis A.14,15 Chronic hepatitis A infections during pregnancy have not been reported.14,16 Although HAV infection is not a risk factor for fetal teratogenicity,17-19 it may cause premature CONTACT Hui Jin © 2016 Taylor & Francis

[email protected]; Pei Liu

[email protected]

KEYWORDS

pregnant women; vaccination; viral hepatitis

contractions, placental separation, and uterine bleeding, which may lead to preterm delivery .20,21 Efficacy and safety of HA vaccines Inactive and live attenuated HA vaccines are used in the general population. Inactive vaccines with a 2-dose schedule, such as Havrix®, Vaqta®, Epaxal®, are effective and safe in children and adults.22-25 Live, attenuated HA vaccines, such as the H2 strain vaccine, are also reportedly immunogenic and safe for children in China26-29 and India.30,31 Several surveys have assessed the safety of inactive HA vaccines before or during pregnancy. One study on the risk of pregnancy outcomes among pregnancies conceived after human papillomavirus virus and HAV vaccination32 reported no obvious evidence to support that HAV vaccination before conception was associated with miscarriage. In the Vaccine Adverse Event Reporting System (VAERS) from 1996 to 2013,33 severe adverse effects were reported in 4.9% and 6.3% of pregnant women who received HA and hepatitis AB vaccines, respectively; the most common adverse pregnancy outcome was spontaneous abortion. While GlaxoSmithKline also registers data on pregnancy and infant outcomes after administration of the hepatitis AB vaccine, no results have been published.33 Additional reliable trials and surveys are necessary to explore the effectiveness and safety of inactive HA vaccines in pregnant women. HA vaccines immunization Several countries, including the United States34 and China,35 recommend routine HA immunization in children
1 year of age, and target vaccination is accepted in high-risk groups,36 such as travelers to regions of intermediate or high

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endemicity.33 The ACIP recommends administration of inactivated HA vaccines during pregnancy only if the benefits outweigh the potential risks,3,7,17,37-39 and inactive HA vaccines during pregnancy should be administered at 0 and 6 months.5 However, while the Food and Drug Administration (FDA) categorizes inactive HA vaccines as C-class drugs in pregnant women,40 the Global Advisory Committee on Vaccine Safety has not drawn any conclusions about HAV vaccination in the pregnant population.41 Furthermore, there is a suggestion that immune globulin is considerable during pregnancy to prevent post exposure.42,43 In the Vaccine Safety Datalink (VSD) project conducted during 2002–2009,40 the rate of HAV vaccination was 2.34/1,000 pregnancies, and HA vaccines were mostly administered during the first trimester to women less than 18 y of age, suggesting that the parents or obstetrics and gynecology specialists may not have been aware of the pregnancies at the time of vaccination.40,44

Hepatitis B Hepatitis B virus (HBV) infection causes the most severe symptoms, and is a major cause of chronic liver disease, cirrhosis, and liver cancer.45 Among pregnant women, hepatitis B is a pre-existing or concurrent liver disease,46 and the clinical symptoms in infected pregnant women are similar to those of non-pregnant women.47,48 HBV infection does not directly threaten maternal or fetal lives;49-55 however, gestational diabetes mellitus, antepartum hemorrhage, and preterm labor have been reported in chronic carriers.56-58 The most significant risk of HBV infection during pregnancy is the potential for viral transmission to the fetus or neonate,7,59-62 which is associated with 4.5 million cases annually.63 More than 90% of neonates with chronic infections received hepatitis B virus from their

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mothers.59,64-66 Therefore, prevention of vertical HBV transmission is important.

Efficacy and safety of HB vaccines There are 2 kinds of Hepatitis B (HB) vaccines: plasma-derived vaccines and recombinant HB vaccines, however, only recombinant HB vaccines are used globally. Recombinant HB vaccines with 3- or 4-dose schedules, such as Engerix-B, are effective and safe for infants67,68 and adults.69-71 To our knowledge, no large-scale randomized controlled trials (RCTs) have yet assessed the efficacy and safety of HB vaccines in pregnant women,72 likely due to ethical issues.8 However, several studies with small numbers of samples have reported the immunity and safety of recombinant HB vaccines73-80 and Heptavax,51,61,81 during pregnancy (Tables 1 and 2), and Heptavax has been replaced by the former vaccines since the 1990s. HBV vaccination during pregnancy is reported to be immunogenic,61,74-77,79,80 with a passive transfer of antibodies to the fetus.61,73,81 However, one study with a limited sample size observed lower anti-HBs titers among infants born to women vaccinated during pregnancy than those born to mothers who acquired immunity before pregnancy,79 an observation that may suggest that pregnant women should be vaccinated before becoming pregnant. Maternal obesity may also interfere with the efficacy of hepatitis B vaccination in pregnant women.75,77 Although data are somewhat limited regarding the safety of HB vaccines during pregnancy, none have reported significantly higher adverse outcomes in vaccinated pregnant women than those who did not receive vaccination; moreover, evidence has shown the major adverse effects of injection to be mild and generally limited to a local reaction.51,77,78 In contrast, one study described adverse pregnancy outcomes in the VAERS database,

Table 1. Vaccination characteristics during pregnancy. Study

Study region/time

HB vaccines Ayoola 198761

Nigeria/—

Levy 199151 Grosheide 199379 # Reddy 1994172 74

Ingardia 1999

Ingardia 199975 77,78

Canada/— Netherlands/1988– 1989 India/— America/1996– 1997 America/1997

Sheffield 2011

Texas/2000–2006

HE vaccine Wu 2012162

China/2007–2009

Study design (sample size)/follow-up Prospective cohort (V:72,C:86 [including 65 anti-HBsC, 21 HBsAgC])/ All (mothers and infants): 12 months after delivery Cohort (10)/All: 1 year after delivery Prospective cohort (16)/ Mothers: 7 months after initial vaccination; infants: 22 months Cohort (15)/ All: for 6 months postdelivery Retrospective cohort (80)/ mothers: 36–40 week of gestation age Retrospective cohort (37)/ All: until delivery Cohort (200)/Mothers: 1–2 months after the third injection RCT (V:36;C:31)/—

Vaccinated pregnant women

Vaccination protocols

Age range: 19–27 y; Gestational age: 3rd trimester

V: Heptavax 20ug/per dose at 0,1month; C: vitamin B at 0, 1 month

All vaccinated at 1st trimester Mean age: 32.5 y; First dose at the 1st trimester: 6/16, Fourth dose after delivery: 9/14. Age range:22–27 y; Gestational age: 2ndand 3rd trimester Healthy gravitas; mean age: 23.8 y

Heptavax RV 10ug/per dose at 0, 1, 2, and 6 months CHBIG (125 IU/ml) at 0, 1 month Heptavax 3 doses at 4–6 weeks intervals RV 20ug/dose at 0, 1, 6 months

Healthy gravidas: HBsAg (¡) and HBsAb (¡) High-risk population; Age range: 16– 45 y; Gestational age at first vaccination: 15 mIU/ml): with 2 doses: 8%; Group Group with 2 doses: 66%; with 3 doses: 6.2%. Group with 3 doses: 100%. No increased neonatal (anti-HBs
10 mIU/ml): 3 dose: — intensive care admission, 90%; 2 doses: 77%; 1 doses: morbidity/mortality 56% compared to general population Congenital anomalies: None

HEV infection: none

—

Notes. subjects were positive for sexually transmitted disease, current injection drug users, or both. Outbreak due to in vitro fertilization treatment. & No evidence to support that adverse pregnancy outcome was related to immunization. RV: recombinant HB vaccines; HB vaccines: hepatitis B vaccines; HE vaccine: hepatitis E vaccine. V: vaccinated group, C: control group. #

reporting that approximately 50% of 88 women reported pregnancy complications, including spontaneous abortions, stillbirths, congenital abnormalities, and preterm labor, although the actual number of cases may be underreported.8 Overall, the available data do not offer consistent findings regarding the efficacy and safety of HB vaccines during pregnancy. HB vaccine immunization The World Health Organization (WHO) recommends that all infants receive the first HB vaccine dose as soon as possible after birth.82 Routine vaccination of infants has been implemented in countries including but not limited to mainland China, Taiwan, Indonesia, and Thailand.60,83-85 The ACIP recommends emergency HB immunization in high-risk pregnant populations6,10,86-89; “high-risk” is defined as having a sex partner positive for hepatitis B surface antigen (HBsAg), having multiple sex partners within the past 6 months, requiring sexually transmitted disease evaluation or treatment, or current or

recent injection drug use.5,7,39 The American College of Obstetricians and Gynecologists (ACOG),90 and the public health agency of Canada88 have approved the recommendations of the ACIP. The HB vaccine is typically administered to women in 3 doses over a period of 6 months before, during, and after pregnancy. Like HA vaccines, the FDA classifies HB vaccines as a C-level drug for pregnant women,40 and the Global Advisory Committee on Vaccine Safety has also not drawn any conclusions about the advisability of HBV vaccination in pregnant population.41 In fact, vaccination in pregnant women is rare. In Mayotte Island, 18.6% of pregnant women have received HB vaccinations.91 In the 2002–2009 VSD, the frequency of HBV vaccination was 3.73/1,000 pregnancies; however, vaccination was possible in cases where the woman and/or provider were unaware of the pregnancy.40 A Chinese study conducted in 2002 reported a lower anti-HB positive rate (56.3%) in pregnant women,92 which may suggest the extended HBV vaccination in women of child-bearing age should be considered.

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Efficacy and safety of Hepatitis B immune globulin (HBIG) Screening of pregnant women and passive-active vaccination at birth may not be effective in preventing intrauterine infection, which typically occurs in the last trimester of pregnancy.52,93 Some reports support administration of HBIG to pregnant women infected with HBV in order to prevent HBV infection in the uterus.94-96 In the UK, HBIG is accepted for mothers positive for hepatitis B e antigen (HBeAg) or with HBV-DNA levels above 1.0£106 IU/mL.97,98 HBIG is also administered to HBsAg-positive mothers in China. A study conducted in district-level hospitals of Wuhan City, China from 2004–2006 reported that 90.5% of HBsAg-positive pregnant women received HBIG.99 Several studies have assessed the use of HBIG during pregnancy for prevention of fetal infection, but its efficiency and safety during pregnancy remain controversial.100 Pregnant women typically receive 200 IU per dose as intramuscular injections once monthly from 28 weeks of gestation. RCTs conducted in China supported the claim that, compared with a control group receiving a placebo or no intervention, HBsAgpositive and/or HBeAg-positive pregnant women receiving HBIG had significantly decreased probability of intrauterine hepatitis B infection,96,101-106 and infants born to mothers administered HBIG during pregnancy had higher HBsAb positive rate at birth and lower prevalence of chronic HBV infection.102 Related to the safety of administration of HBIG during pregnancy, the limited data show no severe adverse effects in mothers or infants.107-112

Hepatitis C Hepatitis C virus (HCV) infection is also an important cause of chronic liver disease, cirrhosis, and liver cancer. An estimated 1–8% of pregnant women worldwide are positive for HCV infection113,114; however, the prevalence of HCV infection in pregnant women is difficult to confirm owing to the lack of large-scale, representative surveys.18,115 Acute HCV infection is usually asymptomatic and rarely reported in pregnant women, 116 but chronic HCV infection is common in pregnancy.18,116 Maternal and neonatal outcomes, including gestational diabetes, preterm delivery, and low birth weights, have been reported.117-120 In addition, vertical transmission plays a major role in pediatric hepatitis C121; the prevalence of mother-tochild transmission from HCV-infected women without HIV infection is an estimated 2–8%,18,115,122,123 and 2–3 times higher in mothers co-infected with HIV. 124-127 There is currently no vaccine for hepatitis C,15,128 and immune globulin is not effective in preventing pre- or postexposure HCV infection.128,129 Moreover, the ACOG recommends HCV screening only for pregnant women with risk factors, such as illegal drug use.90,130

Hepatitis D Hepatitis D infections occur only in the presence of HBV infection.131 An estimated 15 million of 240 million chronic HBV carriers are also infected with hepatitis D virus (HDV).132 Coinfection typically leads to acute HDV infection, while super-

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infection causes chronic infection in more than 90% of cases.133 The disease burden of HDV infection has declined in regions where universal HBV vaccination are carefully designed and efficiently implemented.131,133 Acute HDV infection does not directly lead to death during pregnancy,133,134 but chronic hepatitis D infection may promote HBV-related liver disease;134 thus, hepatitis D is considered one of the most severe forms of viral hepatitis in humans.131,135 There are no HD vaccines or immune globulin to prevent hepatitis D,136 but measures to prevent hepatitis B are also generally effective against HDV infection.16,137 A mathematical model predicted that coverage of HB vaccination to be an important factor influencing the outcome of HDV infection.137

Hepatitis E Hepatitis E virus (HEV) infection is a common cause of non-A, non-B, enterically transmitted acute viral hepatitis worldwide.138 Compared with other types of viral hepatitis, pregnant women have increased risk of HEV infection.139,140 A distinctive feature among pregnant women infected with HEV is high morbidity and mortality due to acute hepatic failure,141-144 and adverse maternal outcomes, such as abortion, premature delivery, stillbirth, and intra-uterine death are common in infected cases.145-148 A survey in rural Bangladesh attributed 9.8% of pregnancy-associated deaths to acute HEV infections;149 Gurley et al.150 concluded that HEV infection was responsible for 58% of deaths in pregnant patients with acute liver disease or fluminant hepatitis in HEV endemic regions. In 2005, the possibility of death in HEV-infected pregnant women was an estimated 0.198, with up to 3,000 stillbirths in 9 Global Burden of Disease regions.151 Moreover, some surveys have observed vertical transmission among infected mothers.152-154 Efficacy and Safety of HE vaccines To date, the 56 KD vaccine155-157 and HEV239 vaccine158,159 have passed phase 2 or 3 clinical trials, and the HEV239 vaccine (Hecolin) is currently commercially available in China.160,161 Only one survey provided a preliminary analysis of the efficacy and safety of incidental immunization during pregnancy in phase 3 trials of the HEV239 vaccine (Tables 1 and 2) with no HEV-infected cases reported among all HE/HB-vaccinated pregnant women in the study of Wu et al.162; the prevalence of adverse effects was similar to non-pregnant women injected with the HEV239 vaccine; moreover, no spontaneous abortions or congenital anomalies were reported in either HE vaccinated or HB vaccinated mothers (placebo group). In addition, immune globulin is not recommended to prevent hepatitis E; although limited, the existing evidence suggests its protective effect on hepatitis E infection.138,163-165 Studies of mouse models have shown HE vaccine candidates, including recombinant neutralizing epitope protein,166 and insect larvae-derived recombinant hepatitis E virus ORF-2 proteins,167 to be well-tolerated, inducing high anti-HEV titers in pregnant mice as well as antibody transfer to offspring167; however Li et al.168 believed that pregnant mice were not an appropriate model to explore the efficacy and safety of HE vaccines because female mice are not vulnerable to HEV infection.

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Conclusion Pregnancy should not be a contraindication to immunization with inactivated vaccines or immune globulin,86 as vaccination of pregnant women protects susceptible or high-risk mothers, fetuses, and infants.3,10 Currently, while the ACIP recommends emergency immunization during pregnancy using inactive HA and HB vaccines,3,7 there are no global policies regarding vaccination during pregnancy. Although HBIG administered to pregnant women infected with HBV can decrease intrauterine infection rates, it is not approved worldwide, possibly due to potential risks or the prohibitive cost of therapy.99,169 Moreover, compared with hepatitis A, B, C, and D, a higher incidence of fulminate hepatitis failure has been observed in pregnant women with HEV infection;15,170 the HEV239 vaccine currently available in China could be a candidate for prevention hepatitis E infection in pregnant women. In addition, due to obstacles regarding vaccine clinical trials in pregnant women, observation studies may be useful to explore the efficacy and safety of vaccination during pregnancy. Thus, national or regional surveillance systems such as the VSD40 may be useful for addressing this problem.

Abbreviations HA vaccine HB vaccine HE vaccine HAV HBV HCV HDV HEV ACIP FDA VSD HBsAg HBeAg HBsAb VAERS HBIG ACOG RCTs

Hepatitis A vaccine Hepatitis B vaccine Hepatitis E vaccine Hepatitis A virus Hepatitis B virus Hepatitis C virus Hepatitis D virus Hepatitis E virus Advisory Committee on Immunization Practices Food and Drug Administration Vaccine Safety Datalink Hepatitis B surface antigen Hepatitis B e antigen Hepatitis B surface antibody Vaccine Adverse Event Reporting System Hepatitis B immune globulin American College of Obstetricians and Gynecologists Randomized controlled trials

Disclosure of potential conflicts of interest The authors declare that there are no potential conflicts of interest.

Funding This study was funded by the National Natural Fund (81573258, 81402769) and the Jiangsu Provincial Social Development Fund (BE2013723, SBE2015710027).

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