HUMAN VACCINES & IMMUNOTHERAPEUTICS 2016, VOL. 12, NO. 4, 857–865 http://dx.doi.org/10.1080/21645515.2015.1101524
REVIEW
Improving rates of maternal immunization: Challenges and opportunities Donna M. MacDougalla,b and Scott A. Halperina a Canadian Center for Vaccinology, Dalhousie University, IWK Health Centre, and Nova Scotia Health Authority, Halifax, Nova Scotia, Canada; bSchool of Nursing, St. Francis Xavier University, Antigonish, Nova Scotia, Canada
ABSTRACT
ARTICLE HISTORY
Objectives: An increasing number of vaccines are recommended or are being developed for use during pregnancy to protect women, fetuses, and/or newborns. For vaccines that are already recommended, vaccine uptake is variable and well below desired target. We reviewed the literature related to factors that affect a healthcare provider’s recommendation and a woman’s willingness to be vaccinated during pregnancy. Design: A scoping review of published literature from 2005 to 2015 was undertaken and all relevant articles were abstracted, summarized, and organized thematically. Results: Barriers and facilitators were identified that either decreased or increased the likelihood of a healthcare provider offering and a pregnant woman accepting vaccination during pregnancy. Concern about the safety of vaccines given during pregnancy was the most often cited barrier among both the public and healthcare providers. Other barriers included doubt about the effectiveness of the vaccine, lack of knowledge about the burden of disease, and not feeling oneself to be at risk of the infection. Major facilitators for maternal immunization included specific safety information about the vaccine in pregnant women, strong national recommendations, and healthcare providers who both recommended and provided the vaccine to their patients. Systems barriers such as inadequate facilities and staffing, vaccine purchase and storage, and reimbursement for vaccination were also cited. Evidence-based interventions were few, and included text messaging reminders, chart reminders, and standing orders. Conclusions: In order to have an effective vaccination program, improvements in the uptake of recommended vaccines during pregnancy are needed. A maternal immunization platform is required that normalizes vaccination practice among obstetrical care providers and is supported by basic and continuing education, communication strategy, and a broad range of research.
Submitted March 8 2015 Revised 17 September 2015 Accepted 25 September 2015
Introduction Vaccination during pregnancy is increasingly being recommended to control infectious diseases that affect pregnant women, fetuses, and newborn infants.1 While there is currently much interest in a maternal immunization platform as a vaccination strategy, the concept is not new. From 1938 to 1951, multiple studies were undertaken to explore the safety and effectiveness of giving the whole-cell pertussis vaccine to pregnant women to provide protection to the newborn infant.2-4 In 1961, tetanus toxoid given to pregnant women was demonstrated to be highly effective in preventing neonatal tetanus.5 Over the last 25 years, routine immunization of pregnant women throughout the developing world has led to >93% reduction in maternal and neonatal tetanus.6 Routine immunization of pregnant women with inactivated influenza vaccine has been recommended in the United States since 1960;7 there is accumulating evidence that this provides benefit not only to the pregnant woman, but also to the fetus8,9 and the newborn infant.10,11 Currently, immunization of pregnant women is recommended in the developing world for tetanus12 and influenza13 and in many developed countries for influenza and pertussis.14 New vaccines are under development and in clinical trials for immunization of pregnant women against group B Streptococcus15 and Respiratory Syncytial Virus.16,17 Although vaccine acceptance and uptake has
Barriers; maternal immunization; opportunities
been strong with tetanus vaccine, vaccine coverage with influenza vaccine and pertussis vaccine has been variable. Maternal influenza vaccination rates in the United States have now risen to approximately 50% and were somewhat higher during the H1N1 pandemic.18 High rates of pertussis vaccination during pregnancy (in excess of 70%) were achieved in the United Kingdom after the program was implemented in response to an increase in neonatal pertussis deaths.19 Similar success has not been achieved in the United States, where rates have been estimated to be below 5% despite 5 y of a maternal immunization recommendation.20 There are a number of barriers to achieving high rates of vaccination coverage within any population.21 Achieving high rates of vaccination among pregnant women presents additional and more complex difficulties. However, a number of opportunities and facilitators may be present that could enhance the success of maternal immunization programs. We describe the challenges and opportunities involved in improving coverage with recommended vaccines for pregnant women.
Results In the 64 publications reviewed, influenza vaccine was the most frequently evaluated vaccine (n D 47); 11 studies addressed the 2009 H1N1 influenza pandemic. More recently, with new
CONTACT Donna M. MacDougall [email protected] Color versions of one or more figures in this article can be found online at www.tandfonline.com/khvi. © 2016 Taylor & Francis
KEYWORDS
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recommendations for the use of Tdap during pregnancy, 10 studies explored factors associated with Tdap vaccine uptake. In contrast, no studies were identified evaluating factors associated with tetanus toxoid acceptance during pregnancy, perhaps related to the location of those universal vaccination programs in low-resource countries and the long-standing existence of those programs. Only one study reported factors predicted to be associated with a vaccine still in development, group B Streptococcus.15 Five studies explored general issues of maternal immunization rather than vaccine-specific issues. Most studies were reported from the United States (n D 37), Australia (n D 10), and Canada (n D 6). One study was reported from each of the United Kingdom, Belgium, Germany, South Korea, Taiwan, and Hong Kong. Most studies involved pregnant women (n D 46); 15 reported on healthcare providers, of which physicians predominated (n D 10). Five studies included nonphysicians (3 with midwives and 2 with obstetrical care providers). A number of barriers that decrease vaccination of pregnant women have been identified as well as facilitators that increase the likelihood of vaccine update during pregnancy. Only a limited number of evaluations of interventions have been described. Barriers, facilitators, and interventions can be categorized into those related to pregnant women, to healthcare providers, to the vaccine itself, and to the health system.
barrier to any immunization, including those given during pregnancy.33,34,37 Barriers external to the women also influenced their decision to be vaccinated or not during pregnancy: inadequate time,34 social norms and family influence,33,50 and religion33 were cited. For influenza vaccine, lack of a strong and unequivocal recommendation by healthcare professionals, government, and advisory bodies also contributed to decreased vaccine uptake among some populations.28,32-34,41,42,46,51,52 Many of the facilitators associated with increased vaccine uptake were the opposite of the barriers identified. High level of vaccine knowledge,28,49,53,54 perceived vaccine effectiveness50 and benefit,41 increased perception of disease severity,39,45 and feeling personal susceptibility42,45,47,50 were predictive of improved vaccine uptake during pregnancy. Having a family physician,24 family influence,34 existing co-morbidities,24 and concern about regretting not getting the vaccine also favorably influenced a woman’s decision to be vaccinated.47,50 The desire to protect the fetus/infant and oneself from disease was a strong predictor of immunization.22,23,29,34,42,46,55,56 Most consistently, having the vaccine recommended AND offered by their healthcare provider21-23,25,28,29,31-34,37-40,42,45,46,50,54-60 and trusting the recommendations47 were identified most frequently as important in increasing vaccine uptake. For influenza vaccine, prior vaccination of oneself25,28,34,45,46,53,60 or one’s partner59 in previous years was a strong predictor of acceptance of vaccination during pregnancy.
Factors related to pregnant women In most studies, certain demographic factors were associated with acceptance of vaccination during pregnancy. Lower uptake was associated with younger age,22-25 having less than a university degree,22,25,26 not being married,22,27 being Hispanic or Black,22,23 lacking health insurance,22,25,26 smoking,24,27 being below the poverty line,22,24 not having an obstetrical care provider,21,23 and having a history of pre-term delivery.22,24,26 Barriers identified by pregnant women included perceptions about disease severity and the risk of the disease, lack of knowledge about and mistrust of vaccines, concerns about vaccine safety and effectiveness, fear of needles, lack of recommendations, and societal factors including social norms, family influence, and religion (Table 1). An increased concern about disease severity increases the likelihood of being immunized during pregnancy,28 while not feeling at risk of the disease decreased the likelihood of immunization.22,29-34 Lack of awareness of personal risk was commonly noted in relation to influenza vaccine, particularly during the 2009 H1N1 pandemic. Lack of knowledge about the disease, vaccine, and risk of infection was commonly cited in studies related to influenza and pertussis.28,29,34-41 Most women identified safety concerns such as side effects as the greatest barrier to immunization during pregnancy.29-32,35-38,42,43,45,46 While women were concerned about their own safety25,30,34,37,44-46,51,52 or prior adverse events with the vaccine,46,47 safety concerns for the fetus and newborn were paramount.22,25,30,31,34,39,44-46,51,52 Doubt about the effectiveness of the vaccine was particularly noted with influenza vaccine.22,25,32,34,35 General mistrust of vaccinations37 was mentioned in studies related to influenza,29 pertussis,30 and group B Streptococcus.49 In some women, fear of needles presented a
Factors related to healthcare providers recommending vaccines Barriers identified that affect healthcare providers’ provision of vaccines during pregnancy were similar to those that affected pregnant women. Lack of knowledge and updated education among providers of obstetrical services was identified frequently as a barrier to implementation of maternal immunization recommendations.29,32,37,60-65 As with pregnant women, misperceptions about the risk of the disease61 and concerns about vaccine safety61,63,66 and efficacy66 and the need for vaccination during pregnancy65 were identified as barriers for healthcare providers. Concern was often raised about lack of studies done specifically with pregnant women. Additional barriers were misperceptions related to their patients’ preferences for vaccination during pregnancy and patient refusal,37,66 lack of time,66 concern about liability and blame,65 ambiguous guidelines,66 uncertainty about who bears the responsibility for vaccine-related discussions with pregnant women,54,65,68 inability to track vaccination status of their pregnant patients,69 solo practice,68 and vaccination not being part of their typical practice.63 Factors that facilitated vaccination and were associated with providing vaccination to patients included a general positive attitude toward vaccination,54 concern about the seriousness of influenza,68 and belief in the safety and efficacy of the vaccines.70 Older providers54 and those who were immunized themselves43,70 were more likely to recommend and provide vaccinations to their pregnant patients. Obstetrical care providers who also provided primary care,63 who believe primary care and preventative medicine are a very important part of
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Table 1. Factors affecting vaccine uptake in pregnant women. Categories Women (receiving vaccines)
Barriers
Facilitators
Concern about vaccine safety. (general, self, baby, side effects). 22,25,29,30-32,34-39,42-46,48,51,52
Vaccine effectiveness and efficacy. 22,25,32,34,35
Vaccine was recommended and offered by HCP.
28,29,34-41 28
Perceived disease severity.
Patient-centered pamphlet.78,79
21-23,25,28,29,31,33,34,37-40,42,45,46,50,54-60
Protect baby and self from disease. 22,23,29,34,42,46,55,56
Lack of vaccine knowledge.
Interventions
Have the flu shot in a previous year/or last 2 y.25,28,34,45,46,53,60 High level of vaccine knowledge.
Text messaging with general pregnancy health and vaccination information, and appointment reminders.81,82 Text4baby mobile health program.83 Teach-back method.80
28,49,53,54
Lack of recommendation to receive vaccine.
Anticipated inaction regret.47,50
28,32-34,41,42,46,51,52,59
Perceived risk of disease.22,29-34 Lack of trust in the vaccine.29,30,37,49 Social norms and family influence.33,50 Fear of the vaccine/needles.33,34,37 Religion.33 Previous adverse reaction.46,47 Time.34 Will give me the flu.25 Healthcare providers (recommending vaccines)
Lack of knowledge/education. 29,32,37,60-65 61,63,66
54
Vaccine safety.
Increased age of provider.
Perceived risk of disease.61 61
Lack of vaccine testing.
Tracking patient vaccination status.69 Uncertainty about who bears the responsibility for vaccination discussions/vaccine governance.54,65,68 Physician in solo practice.68 Misperceptions about what the patient wants.37 Not usual practice to vaccinate.63 Patient refusal.66
Vaccine Systems
Perceived vaccine effectiveness.50 Existing comorbidities.24 Having a family physician.24 Felt susceptible to infection.42,45,47,50 Perceived infection severity.39,45 Working in a high-risk environment.34,46 Partner recently vaccinated.59 Perceived vaccine benefits.41 Information from the family.34 Trust recommended guidelines.47 National recommendation provided.30
Ambiguous guidelines.66 Vaccine efficacy.66 Lack of time.66 Risk of blame if adverse event occurs.65 Unconvinced of need.65 Before a vaccine exists, knowledge likely very unimportant; if it exists, hesitancy issues enter.49 Reimbursement.62-64,66,68 Liability.64,66 Compliance with reporting.64 Access to care.37,39,41,59 Vaccine tracking.64 Ineffective dissemination of information from clinics to patients.28 Cost of vaccine to patients.59,62 Cost of ordering vaccine and maintaining supply, and storage. 32,63,66,68
Lack of staff.66 Workload.65 Work setting unsuitable.65
Belief in the safety and efficacy of the vaccines.70 If immunized themselves.43,70 Providing primary care.63 Engagement with the flu program.71 Practising in a multispecialty group.68 Positive attitudes about vaccination.54 Belief primary care and preventative medicine are a very important part of practice.68 Observing serious conditions attributed to influenza-like illness (ILI).68
Incorporation of maternal immunization into standard care through a structured process.73 IT involvement with timely monitoring of program.71 Access to a clinic-based setting.57 Single dose preferred.49 Timing of vaccine delivery (not in first trimester).49
Chart reminders and physician education.74 Physician education program and distributed posters.78 Best practice alert.75 Physician opt-in orders and standing orders.77 Computer decision support.76
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their practice,68 who practised in a multispecialty group,68 and who were more engaged with the public influenza program71 were also more likely to provide influenza vaccine to pregnant women. As with pregnant women, existence of national recommendations increased the likelihood of vaccination in pregnancy by obstetrical healthcare providers.30 Factors related to the vaccine and immunization systems Both pregnant women and obstetrical care providers were cautious about the use of vaccines that had not been in widespread use for several years.49 For vaccines that were still under development (e.g., group B Streptococcus), knowledge gaps seemed to be less of a concern than the unproven nature of the vaccine. Similar concerns were raised over the novelty of the H1N1 pandemic vaccines, particularly in relation to the use of novel adjuvants.32,38,44,56,61,72 Once a vaccine was in common use (e.g., Tdap, seasonal influenza vaccine), common issues related to vaccine hesitancy become more dominant.49 Health systems barriers were identified by both pregnant women and healthcare providers. Depending on the jurisdiction and the method of financing healthcare delivery, substantial economic barriers to immunization during pregnancy were identified. Workload, lack of staff65,66 and suitable practice setting,65 reimbursement of obstetrical care providers for the cost of ordering the vaccine and maintaining its supply,32,63,66,68 vaccination status tracking, and compliance with reporting64 were barriers identified by practitioners. Concern was raised about increased liability related to providing vaccination services.64,66 For pregnant women, access to vaccination services37,39,41,59 and having to pay for the vaccine and administration costs were barriers to immunization during pregnancy.37,59,62 Lack of effective communication and dissemination of recommendations from care providers, clinics, and public health to pregnant women were noted to be barriers during the 2009 H1N1 pandemic.29 Health systems innovations that acted as facilitators to improved vaccine coverage during pregnancy were also identified. Incorporation of maternal immunization into standard obstetrical care73 and access to more convenient clinic settings57 improved access for pregnant women. Information technology support with timely monitoring of program successes and challenges improved rates of vaccine uptake during pregnancy.71 For new vaccines, single-dose schedules and avoiding administration of vaccines during the first trimester were identified as mechanisms to improve vaccine acceptance.49 Interventions While many barriers and facilitators to implementation of a maternal immunization platform have been identified, evidence-based interventions to improve vaccine coverage are limited to date. Chart reminders and physician education were associated with substantial improvements in vaccine coverage in 6 obstetrical care provider practices; rates increased more dramatically among family physicians than among obstetricians.74 Although it was a prospective study, the controls were historical rather than concurrent, and the results could have been confounded by overall improvement in maternal
immunization coverage rates during that time. Benefits were also demonstrated in a study of “best practice alerts” in charts that also use a pre- and post-intervention analysis.75 A computer decision support algorithm that aided in identifying women needing immunization was found to be an effective intervention in a hospital-based clinic,76 and opt-in and standing orders for vaccination have also been shown to be effective.77 Patient78,79 and physician education74,78 have also been shown to increase vaccine uptake rates, although several of the previously cited chart alert interventions were implemented after failure of physician education programs.75,76 A “teach back” method of providing health information was assessed in Jamaica, and its success was associated with health literacy which was closely correlated with overall literacy.80 Studies of text messaging reminders have had mixed results. In a 2013 randomized controlled trial, influenza vaccination rates were not different in the group that received 12 weekly text messages encouraging general pregnancy health and influenza immunization.81 In contrast, in a 2014 randomized controlled trial, text message reminders about influenza vaccination were associated with an increase in influenza immunization, particularly among those who received the messages early in their third trimester.82 A mobile app for smart phones that sent automated text messages also increased vaccine uptake during pregnancy.83
Discussion and commentary Maternal immunization for protection of the pregnant woman, the fetus, and the newborn is being recommended for an increasing number of existing vaccines, and new vaccines are being developed specifically for this purpose. Acceptance of this effective intervention by both the public and healthcare providers encounters a number of obstacles related to the attitudes and beliefs of pregnant women and healthcare providers and to the healthcare system itself. Overcoming these barriers is essential in order to improve the quality of obstetrical care and enable women to access immunizations as a routine part of their preventative care.1 Most of the barriers that have been identified relate to influenza vaccine, primarily due to the longstanding recommendation for the immunization of all pregnant women with influenza vaccine. However, many of the barriers are applicable to Tdap vaccine, which is now universally recommended during pregnancy in a number of countries. While there are some differences between vaccines that have a longstanding safety record and novel vaccines, strategies that are implemented to overcome barriers to use of these longstanding vaccines will likely be applicable for all vaccines added to a new maternal vaccination platform. For pregnant women, the most significant barrier to vaccine uptake is concern about the safety of the vaccine for themselves and, more importantly, for their fetus and newborn. The novelty of the immunization recommendation in the face of longstanding exhortations to avoid all medications during pregnancy and the lack of safety data generated specifically in pregnant women adds to the concern that vaccination during pregnancy is a risky endeavor. Lack of knowledge about the severity and burden of disease compounds the problem, which is further exacerbated by general distrust of the healthcare system. Paradoxically, lack of strong, clear recommendations by health authorities is also
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commonly cited as a barrier. While not a major factor, social norms and family and friends’ opinions also affect a woman’s decision making regarding vaccination. For healthcare providers, lack of knowledge and lack of national recommendations also affect their willingness to deliver vaccines to pregnant women and the strength of their personal recommendation to their patients. More often cited as a barrier were issues related to their practice; delivery of vaccinations has not traditionally been in the purview of obstetrical care providers, and the logistics of vaccine acquisition, storage, administration, and tracking are daunting for many practitioners. Higher rates of delivery of vaccination during pregnancy were demonstrated by family physicians who provide obstetrical care, likely because vaccination is a standard part of their non-obstetrical practice. In a call to action by the US National Vaccine Advisory Committee (NVAC), a number of gaps were identified that need to be addressed in order to deliver a coordinated maternal immunization strategy.1 The Committee recommended that an enhanced communication strategy was required to address the safety and effectiveness of vaccination during pregnancy, addressing the underlying motivations as to why a patient gets immunized and factors contributing to vaccine hesitancy. Communication to healthcare providers was also deemed essential, with provision of ongoing and timely updates to the full range of healthcare providers who deliver obstetrical care. While publicly presented information is important (websites, brochures, etc.), it is essential that front-line care providers be educated to be sources of trusted vaccination information and advocates of maternal immunization policies. Improvements are required to these publicly available resources. Multiple media systems, including traditional and social media, need to be exploited and the messages coordinated. One-size messaging and use of a single medium will no longer reach a sufficiently broad audience. Pregnancy websites, mobile technologies, texting, reminder messages, magazines, newspapers, radio, and TV all have a role to play as public information sources become increasingly fragmented. In the US, NVAC advocates a role for the federal government in this coordinating activity. Although honed for the specific audiences, the messages provided by different organizations should be unified in theme and recommendation. Communication is not sufficient; systemic changes are needed in order to improve rates of maternal immunization. Vaccination must become a part of the fiber of routine obstetrical care, much as it has for pediatric care over the last 50 y. Formalizing a maternal immunization strategy is an important step in normalizing provision of vaccination by obstetricians, midwives, family physicians, and other obstetrical care providers. Specific, evidence-based guidelines are needed, and all care providers should be encouraged to adhere to them as a routine part of their practice. Office-based practices that support the routine delivery of vaccines should be part of all obstetrical practices. Vaccines need to be both recommended AND provided by those delivering obstetrical care in all practices settings. Curricula should be developed for trainees about the risks and benefits of immunization during pregnancy and postpartum, and vaccination competency should be an expected requirement of training programs for all obstetrical care providers. Access to
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vaccine registries by obstetrical providers is critical to being able to monitor an individual woman’s vaccination status as well as to measure the rates of vaccine coverage achieved by each obstetrical care practice. Missed opportunities for vaccination should be identified in this manner and feedback mechanisms implemented in order to improve the quality of the maternal immunization platform among individuals and practices. The movement to electronic medical records can facilitate this process and contribute to improved vaccination coverage. Issues regarding funding for maternal immunization programs should be addressed in each jurisdiction to ensure that access to vaccination during pregnancy is available to all women and that providers are compensated for the cost of delivering the vaccination program. Liability concerns need to be addressed for practitioners as well as for vaccine manufacturers, some of whom are still reluctant to undertake the necessary clinical trials to provide the safety and efficacy data which the public, providers, and regulators need in order to be comfortable with maternal immunization recommendations. These ongoing research needs must be met to support the recommendations and to inform their expansion to other disease targets. Understanding the mechanism of protection provided by maternal immunization, the duration of protection, the optimal timing of immunization during pregnancy, the need for repeat dosing in subsequent pregnancies, and the effect of maternal-derived antibodies on the active immune response in the newborn are just some of the information that is needed to support maternal immunization programs. As well, there is a critical need for implementation research to determine what interventions are effective in addressing the concerns of the public and healthcare providers, recognizing the diversity of stakeholders comprising even a single one of these groups. In summary, maternal immunization as a strategy to protect pregnant women, fetuses, and newborns will be most effective by establishing a formal maternal immunization platform similar to the infant and adolescent programs that have achieved remarkable successes (Figure 1). In order to have a significant impact on the disease burden on newborns, implementation of the strategy at national and international levels is needed, with leadership taken by each jurisdiction’s technical advisory group. This new platform must be integrated into the routine practice of all obstetrical care providers, through extensive education in training programs and ongoing continuing education programs. Communication to the public is essential, and understanding and addressing the concerns of pregnant women is fundamental to the success of the intervention. While a number of interventions have been studied, most strategies lack data supporting their effectiveness; the lack of evidence-based recommendations fuels doubt among both the public and providers and weakens the strength of vaccination recommendations. A coordinated strategy must be implemented in order to achieve high rates of maternal immunization coverage.
Methods The focus of this review was to provide an overview of the effect of knowledge, attitudes, and practices of pregnant women and their healthcare providers on improving uptake of vaccines that are recommended during pregnancy.
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Literature search We identified potentially eligible reports by searching the following databases on June 8, 2015: CINAHL, PubMed, Science Direct, Springer Link, ProQuest, Oxford Journals, Taylor and Francis, Wiley, and Google Scholar via the Web of Knowledge. Search terms were identified and then corroborated using the index of keywords for each database. Our search terms were “maternal vaccination," “maternal immunization (immunisation)," “vaccination," “immunization (immunisation)," “pregnancy," “uptake," “education," “attitudes," “promotion” and /or “interventions." The search was limited to articles published in English between 2005 and 2015. We also keyed the titles of relevant articles into the PubMed “related articles” feature to
identify similar reports and into the “times cited” feature in the Web of Knowledge. In addition, we completed a manual search by reviewing the reference lists of all included articles for additional studies. The initial inclusion criteria were articles in English involving vaccination during pregnancy. A relatively small range of research-based articles and reports were retrieved. In total, 95 citations using the search terms were identified from the following sources: CINAHL (5), PubMed (36), Science Direct (10), Springer Link (3), ProQuest (3), Oxford Journals (3), Taylor and Francis (4), Wiley (2), and Google Scholar via the Web of Knowledge (14), and manual search (15). Two reviewers (SAH and DMM) assessed the abstracts. A data collection form was used to abstract data from the studies independently. The form covered information about
Figure 1. Supports required for the establishment of a “maternal immunization platform.” HIC: High-income countries; LMIC: Low- and middle-income countries; RSV: Respiratory Syncytial Virus; Tdap: Tetanus, diphtheria, and acellular pertussis vaccine
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study design, setting, aim of the study, population studied, outcome measures, and important results that identified barriers, facilitators, and logistical information. The reviewers discussed any discrepancies in their results to reach agreement. Very few papers were identified that described intervention-based research (nD10). Both qualitative and quantitative studies including systematic reviews were included in this review. Thirty-one studies were eliminated because they focused on postpartum immunization rather than immunization during pregnancy. Sixty-four articles were eligible for inclusion, meeting our criteria which addressed our primary objective of describing the effect of knowledge, attitudes, and practices of pregnant women and their healthcare providers on improving the uptake of vaccines that are recommended during pregnancy. To be included, the study needed to specify the vaccine used, location, and population studied. We excluded studies that did not address factors that affected uptake of recommended vaccines during pregnancy and vaccine coverage rates. Duplicates were not extracted as well as papers that did not meet the inclusion criteria.
Disclosure of potential conflicts of interest No potential conflicts of interest were disclosed.
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REVIEW
Improving rates of maternal immunization: Challenges and opportunities Donna M. MacDougalla,b and Scott A. Halperina a Canadian Center for Vaccinology, Dalhousie University, IWK Health Centre, and Nova Scotia Health Authority, Halifax, Nova Scotia, Canada; bSchool of Nursing, St. Francis Xavier University, Antigonish, Nova Scotia, Canada
ABSTRACT
ARTICLE HISTORY
Objectives: An increasing number of vaccines are recommended or are being developed for use during pregnancy to protect women, fetuses, and/or newborns. For vaccines that are already recommended, vaccine uptake is variable and well below desired target. We reviewed the literature related to factors that affect a healthcare provider’s recommendation and a woman’s willingness to be vaccinated during pregnancy. Design: A scoping review of published literature from 2005 to 2015 was undertaken and all relevant articles were abstracted, summarized, and organized thematically. Results: Barriers and facilitators were identified that either decreased or increased the likelihood of a healthcare provider offering and a pregnant woman accepting vaccination during pregnancy. Concern about the safety of vaccines given during pregnancy was the most often cited barrier among both the public and healthcare providers. Other barriers included doubt about the effectiveness of the vaccine, lack of knowledge about the burden of disease, and not feeling oneself to be at risk of the infection. Major facilitators for maternal immunization included specific safety information about the vaccine in pregnant women, strong national recommendations, and healthcare providers who both recommended and provided the vaccine to their patients. Systems barriers such as inadequate facilities and staffing, vaccine purchase and storage, and reimbursement for vaccination were also cited. Evidence-based interventions were few, and included text messaging reminders, chart reminders, and standing orders. Conclusions: In order to have an effective vaccination program, improvements in the uptake of recommended vaccines during pregnancy are needed. A maternal immunization platform is required that normalizes vaccination practice among obstetrical care providers and is supported by basic and continuing education, communication strategy, and a broad range of research.
Submitted March 8 2015 Revised 17 September 2015 Accepted 25 September 2015
Introduction Vaccination during pregnancy is increasingly being recommended to control infectious diseases that affect pregnant women, fetuses, and newborn infants.1 While there is currently much interest in a maternal immunization platform as a vaccination strategy, the concept is not new. From 1938 to 1951, multiple studies were undertaken to explore the safety and effectiveness of giving the whole-cell pertussis vaccine to pregnant women to provide protection to the newborn infant.2-4 In 1961, tetanus toxoid given to pregnant women was demonstrated to be highly effective in preventing neonatal tetanus.5 Over the last 25 years, routine immunization of pregnant women throughout the developing world has led to >93% reduction in maternal and neonatal tetanus.6 Routine immunization of pregnant women with inactivated influenza vaccine has been recommended in the United States since 1960;7 there is accumulating evidence that this provides benefit not only to the pregnant woman, but also to the fetus8,9 and the newborn infant.10,11 Currently, immunization of pregnant women is recommended in the developing world for tetanus12 and influenza13 and in many developed countries for influenza and pertussis.14 New vaccines are under development and in clinical trials for immunization of pregnant women against group B Streptococcus15 and Respiratory Syncytial Virus.16,17 Although vaccine acceptance and uptake has
Barriers; maternal immunization; opportunities
been strong with tetanus vaccine, vaccine coverage with influenza vaccine and pertussis vaccine has been variable. Maternal influenza vaccination rates in the United States have now risen to approximately 50% and were somewhat higher during the H1N1 pandemic.18 High rates of pertussis vaccination during pregnancy (in excess of 70%) were achieved in the United Kingdom after the program was implemented in response to an increase in neonatal pertussis deaths.19 Similar success has not been achieved in the United States, where rates have been estimated to be below 5% despite 5 y of a maternal immunization recommendation.20 There are a number of barriers to achieving high rates of vaccination coverage within any population.21 Achieving high rates of vaccination among pregnant women presents additional and more complex difficulties. However, a number of opportunities and facilitators may be present that could enhance the success of maternal immunization programs. We describe the challenges and opportunities involved in improving coverage with recommended vaccines for pregnant women.
Results In the 64 publications reviewed, influenza vaccine was the most frequently evaluated vaccine (n D 47); 11 studies addressed the 2009 H1N1 influenza pandemic. More recently, with new
CONTACT Donna M. MacDougall [email protected] Color versions of one or more figures in this article can be found online at www.tandfonline.com/khvi. © 2016 Taylor & Francis
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recommendations for the use of Tdap during pregnancy, 10 studies explored factors associated with Tdap vaccine uptake. In contrast, no studies were identified evaluating factors associated with tetanus toxoid acceptance during pregnancy, perhaps related to the location of those universal vaccination programs in low-resource countries and the long-standing existence of those programs. Only one study reported factors predicted to be associated with a vaccine still in development, group B Streptococcus.15 Five studies explored general issues of maternal immunization rather than vaccine-specific issues. Most studies were reported from the United States (n D 37), Australia (n D 10), and Canada (n D 6). One study was reported from each of the United Kingdom, Belgium, Germany, South Korea, Taiwan, and Hong Kong. Most studies involved pregnant women (n D 46); 15 reported on healthcare providers, of which physicians predominated (n D 10). Five studies included nonphysicians (3 with midwives and 2 with obstetrical care providers). A number of barriers that decrease vaccination of pregnant women have been identified as well as facilitators that increase the likelihood of vaccine update during pregnancy. Only a limited number of evaluations of interventions have been described. Barriers, facilitators, and interventions can be categorized into those related to pregnant women, to healthcare providers, to the vaccine itself, and to the health system.
barrier to any immunization, including those given during pregnancy.33,34,37 Barriers external to the women also influenced their decision to be vaccinated or not during pregnancy: inadequate time,34 social norms and family influence,33,50 and religion33 were cited. For influenza vaccine, lack of a strong and unequivocal recommendation by healthcare professionals, government, and advisory bodies also contributed to decreased vaccine uptake among some populations.28,32-34,41,42,46,51,52 Many of the facilitators associated with increased vaccine uptake were the opposite of the barriers identified. High level of vaccine knowledge,28,49,53,54 perceived vaccine effectiveness50 and benefit,41 increased perception of disease severity,39,45 and feeling personal susceptibility42,45,47,50 were predictive of improved vaccine uptake during pregnancy. Having a family physician,24 family influence,34 existing co-morbidities,24 and concern about regretting not getting the vaccine also favorably influenced a woman’s decision to be vaccinated.47,50 The desire to protect the fetus/infant and oneself from disease was a strong predictor of immunization.22,23,29,34,42,46,55,56 Most consistently, having the vaccine recommended AND offered by their healthcare provider21-23,25,28,29,31-34,37-40,42,45,46,50,54-60 and trusting the recommendations47 were identified most frequently as important in increasing vaccine uptake. For influenza vaccine, prior vaccination of oneself25,28,34,45,46,53,60 or one’s partner59 in previous years was a strong predictor of acceptance of vaccination during pregnancy.
Factors related to pregnant women In most studies, certain demographic factors were associated with acceptance of vaccination during pregnancy. Lower uptake was associated with younger age,22-25 having less than a university degree,22,25,26 not being married,22,27 being Hispanic or Black,22,23 lacking health insurance,22,25,26 smoking,24,27 being below the poverty line,22,24 not having an obstetrical care provider,21,23 and having a history of pre-term delivery.22,24,26 Barriers identified by pregnant women included perceptions about disease severity and the risk of the disease, lack of knowledge about and mistrust of vaccines, concerns about vaccine safety and effectiveness, fear of needles, lack of recommendations, and societal factors including social norms, family influence, and religion (Table 1). An increased concern about disease severity increases the likelihood of being immunized during pregnancy,28 while not feeling at risk of the disease decreased the likelihood of immunization.22,29-34 Lack of awareness of personal risk was commonly noted in relation to influenza vaccine, particularly during the 2009 H1N1 pandemic. Lack of knowledge about the disease, vaccine, and risk of infection was commonly cited in studies related to influenza and pertussis.28,29,34-41 Most women identified safety concerns such as side effects as the greatest barrier to immunization during pregnancy.29-32,35-38,42,43,45,46 While women were concerned about their own safety25,30,34,37,44-46,51,52 or prior adverse events with the vaccine,46,47 safety concerns for the fetus and newborn were paramount.22,25,30,31,34,39,44-46,51,52 Doubt about the effectiveness of the vaccine was particularly noted with influenza vaccine.22,25,32,34,35 General mistrust of vaccinations37 was mentioned in studies related to influenza,29 pertussis,30 and group B Streptococcus.49 In some women, fear of needles presented a
Factors related to healthcare providers recommending vaccines Barriers identified that affect healthcare providers’ provision of vaccines during pregnancy were similar to those that affected pregnant women. Lack of knowledge and updated education among providers of obstetrical services was identified frequently as a barrier to implementation of maternal immunization recommendations.29,32,37,60-65 As with pregnant women, misperceptions about the risk of the disease61 and concerns about vaccine safety61,63,66 and efficacy66 and the need for vaccination during pregnancy65 were identified as barriers for healthcare providers. Concern was often raised about lack of studies done specifically with pregnant women. Additional barriers were misperceptions related to their patients’ preferences for vaccination during pregnancy and patient refusal,37,66 lack of time,66 concern about liability and blame,65 ambiguous guidelines,66 uncertainty about who bears the responsibility for vaccine-related discussions with pregnant women,54,65,68 inability to track vaccination status of their pregnant patients,69 solo practice,68 and vaccination not being part of their typical practice.63 Factors that facilitated vaccination and were associated with providing vaccination to patients included a general positive attitude toward vaccination,54 concern about the seriousness of influenza,68 and belief in the safety and efficacy of the vaccines.70 Older providers54 and those who were immunized themselves43,70 were more likely to recommend and provide vaccinations to their pregnant patients. Obstetrical care providers who also provided primary care,63 who believe primary care and preventative medicine are a very important part of
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Table 1. Factors affecting vaccine uptake in pregnant women. Categories Women (receiving vaccines)
Barriers
Facilitators
Concern about vaccine safety. (general, self, baby, side effects). 22,25,29,30-32,34-39,42-46,48,51,52
Vaccine effectiveness and efficacy. 22,25,32,34,35
Vaccine was recommended and offered by HCP.
28,29,34-41 28
Perceived disease severity.
Patient-centered pamphlet.78,79
21-23,25,28,29,31,33,34,37-40,42,45,46,50,54-60
Protect baby and self from disease. 22,23,29,34,42,46,55,56
Lack of vaccine knowledge.
Interventions
Have the flu shot in a previous year/or last 2 y.25,28,34,45,46,53,60 High level of vaccine knowledge.
Text messaging with general pregnancy health and vaccination information, and appointment reminders.81,82 Text4baby mobile health program.83 Teach-back method.80
28,49,53,54
Lack of recommendation to receive vaccine.
Anticipated inaction regret.47,50
28,32-34,41,42,46,51,52,59
Perceived risk of disease.22,29-34 Lack of trust in the vaccine.29,30,37,49 Social norms and family influence.33,50 Fear of the vaccine/needles.33,34,37 Religion.33 Previous adverse reaction.46,47 Time.34 Will give me the flu.25 Healthcare providers (recommending vaccines)
Lack of knowledge/education. 29,32,37,60-65 61,63,66
54
Vaccine safety.
Increased age of provider.
Perceived risk of disease.61 61
Lack of vaccine testing.
Tracking patient vaccination status.69 Uncertainty about who bears the responsibility for vaccination discussions/vaccine governance.54,65,68 Physician in solo practice.68 Misperceptions about what the patient wants.37 Not usual practice to vaccinate.63 Patient refusal.66
Vaccine Systems
Perceived vaccine effectiveness.50 Existing comorbidities.24 Having a family physician.24 Felt susceptible to infection.42,45,47,50 Perceived infection severity.39,45 Working in a high-risk environment.34,46 Partner recently vaccinated.59 Perceived vaccine benefits.41 Information from the family.34 Trust recommended guidelines.47 National recommendation provided.30
Ambiguous guidelines.66 Vaccine efficacy.66 Lack of time.66 Risk of blame if adverse event occurs.65 Unconvinced of need.65 Before a vaccine exists, knowledge likely very unimportant; if it exists, hesitancy issues enter.49 Reimbursement.62-64,66,68 Liability.64,66 Compliance with reporting.64 Access to care.37,39,41,59 Vaccine tracking.64 Ineffective dissemination of information from clinics to patients.28 Cost of vaccine to patients.59,62 Cost of ordering vaccine and maintaining supply, and storage. 32,63,66,68
Lack of staff.66 Workload.65 Work setting unsuitable.65
Belief in the safety and efficacy of the vaccines.70 If immunized themselves.43,70 Providing primary care.63 Engagement with the flu program.71 Practising in a multispecialty group.68 Positive attitudes about vaccination.54 Belief primary care and preventative medicine are a very important part of practice.68 Observing serious conditions attributed to influenza-like illness (ILI).68
Incorporation of maternal immunization into standard care through a structured process.73 IT involvement with timely monitoring of program.71 Access to a clinic-based setting.57 Single dose preferred.49 Timing of vaccine delivery (not in first trimester).49
Chart reminders and physician education.74 Physician education program and distributed posters.78 Best practice alert.75 Physician opt-in orders and standing orders.77 Computer decision support.76
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their practice,68 who practised in a multispecialty group,68 and who were more engaged with the public influenza program71 were also more likely to provide influenza vaccine to pregnant women. As with pregnant women, existence of national recommendations increased the likelihood of vaccination in pregnancy by obstetrical healthcare providers.30 Factors related to the vaccine and immunization systems Both pregnant women and obstetrical care providers were cautious about the use of vaccines that had not been in widespread use for several years.49 For vaccines that were still under development (e.g., group B Streptococcus), knowledge gaps seemed to be less of a concern than the unproven nature of the vaccine. Similar concerns were raised over the novelty of the H1N1 pandemic vaccines, particularly in relation to the use of novel adjuvants.32,38,44,56,61,72 Once a vaccine was in common use (e.g., Tdap, seasonal influenza vaccine), common issues related to vaccine hesitancy become more dominant.49 Health systems barriers were identified by both pregnant women and healthcare providers. Depending on the jurisdiction and the method of financing healthcare delivery, substantial economic barriers to immunization during pregnancy were identified. Workload, lack of staff65,66 and suitable practice setting,65 reimbursement of obstetrical care providers for the cost of ordering the vaccine and maintaining its supply,32,63,66,68 vaccination status tracking, and compliance with reporting64 were barriers identified by practitioners. Concern was raised about increased liability related to providing vaccination services.64,66 For pregnant women, access to vaccination services37,39,41,59 and having to pay for the vaccine and administration costs were barriers to immunization during pregnancy.37,59,62 Lack of effective communication and dissemination of recommendations from care providers, clinics, and public health to pregnant women were noted to be barriers during the 2009 H1N1 pandemic.29 Health systems innovations that acted as facilitators to improved vaccine coverage during pregnancy were also identified. Incorporation of maternal immunization into standard obstetrical care73 and access to more convenient clinic settings57 improved access for pregnant women. Information technology support with timely monitoring of program successes and challenges improved rates of vaccine uptake during pregnancy.71 For new vaccines, single-dose schedules and avoiding administration of vaccines during the first trimester were identified as mechanisms to improve vaccine acceptance.49 Interventions While many barriers and facilitators to implementation of a maternal immunization platform have been identified, evidence-based interventions to improve vaccine coverage are limited to date. Chart reminders and physician education were associated with substantial improvements in vaccine coverage in 6 obstetrical care provider practices; rates increased more dramatically among family physicians than among obstetricians.74 Although it was a prospective study, the controls were historical rather than concurrent, and the results could have been confounded by overall improvement in maternal
immunization coverage rates during that time. Benefits were also demonstrated in a study of “best practice alerts” in charts that also use a pre- and post-intervention analysis.75 A computer decision support algorithm that aided in identifying women needing immunization was found to be an effective intervention in a hospital-based clinic,76 and opt-in and standing orders for vaccination have also been shown to be effective.77 Patient78,79 and physician education74,78 have also been shown to increase vaccine uptake rates, although several of the previously cited chart alert interventions were implemented after failure of physician education programs.75,76 A “teach back” method of providing health information was assessed in Jamaica, and its success was associated with health literacy which was closely correlated with overall literacy.80 Studies of text messaging reminders have had mixed results. In a 2013 randomized controlled trial, influenza vaccination rates were not different in the group that received 12 weekly text messages encouraging general pregnancy health and influenza immunization.81 In contrast, in a 2014 randomized controlled trial, text message reminders about influenza vaccination were associated with an increase in influenza immunization, particularly among those who received the messages early in their third trimester.82 A mobile app for smart phones that sent automated text messages also increased vaccine uptake during pregnancy.83
Discussion and commentary Maternal immunization for protection of the pregnant woman, the fetus, and the newborn is being recommended for an increasing number of existing vaccines, and new vaccines are being developed specifically for this purpose. Acceptance of this effective intervention by both the public and healthcare providers encounters a number of obstacles related to the attitudes and beliefs of pregnant women and healthcare providers and to the healthcare system itself. Overcoming these barriers is essential in order to improve the quality of obstetrical care and enable women to access immunizations as a routine part of their preventative care.1 Most of the barriers that have been identified relate to influenza vaccine, primarily due to the longstanding recommendation for the immunization of all pregnant women with influenza vaccine. However, many of the barriers are applicable to Tdap vaccine, which is now universally recommended during pregnancy in a number of countries. While there are some differences between vaccines that have a longstanding safety record and novel vaccines, strategies that are implemented to overcome barriers to use of these longstanding vaccines will likely be applicable for all vaccines added to a new maternal vaccination platform. For pregnant women, the most significant barrier to vaccine uptake is concern about the safety of the vaccine for themselves and, more importantly, for their fetus and newborn. The novelty of the immunization recommendation in the face of longstanding exhortations to avoid all medications during pregnancy and the lack of safety data generated specifically in pregnant women adds to the concern that vaccination during pregnancy is a risky endeavor. Lack of knowledge about the severity and burden of disease compounds the problem, which is further exacerbated by general distrust of the healthcare system. Paradoxically, lack of strong, clear recommendations by health authorities is also
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commonly cited as a barrier. While not a major factor, social norms and family and friends’ opinions also affect a woman’s decision making regarding vaccination. For healthcare providers, lack of knowledge and lack of national recommendations also affect their willingness to deliver vaccines to pregnant women and the strength of their personal recommendation to their patients. More often cited as a barrier were issues related to their practice; delivery of vaccinations has not traditionally been in the purview of obstetrical care providers, and the logistics of vaccine acquisition, storage, administration, and tracking are daunting for many practitioners. Higher rates of delivery of vaccination during pregnancy were demonstrated by family physicians who provide obstetrical care, likely because vaccination is a standard part of their non-obstetrical practice. In a call to action by the US National Vaccine Advisory Committee (NVAC), a number of gaps were identified that need to be addressed in order to deliver a coordinated maternal immunization strategy.1 The Committee recommended that an enhanced communication strategy was required to address the safety and effectiveness of vaccination during pregnancy, addressing the underlying motivations as to why a patient gets immunized and factors contributing to vaccine hesitancy. Communication to healthcare providers was also deemed essential, with provision of ongoing and timely updates to the full range of healthcare providers who deliver obstetrical care. While publicly presented information is important (websites, brochures, etc.), it is essential that front-line care providers be educated to be sources of trusted vaccination information and advocates of maternal immunization policies. Improvements are required to these publicly available resources. Multiple media systems, including traditional and social media, need to be exploited and the messages coordinated. One-size messaging and use of a single medium will no longer reach a sufficiently broad audience. Pregnancy websites, mobile technologies, texting, reminder messages, magazines, newspapers, radio, and TV all have a role to play as public information sources become increasingly fragmented. In the US, NVAC advocates a role for the federal government in this coordinating activity. Although honed for the specific audiences, the messages provided by different organizations should be unified in theme and recommendation. Communication is not sufficient; systemic changes are needed in order to improve rates of maternal immunization. Vaccination must become a part of the fiber of routine obstetrical care, much as it has for pediatric care over the last 50 y. Formalizing a maternal immunization strategy is an important step in normalizing provision of vaccination by obstetricians, midwives, family physicians, and other obstetrical care providers. Specific, evidence-based guidelines are needed, and all care providers should be encouraged to adhere to them as a routine part of their practice. Office-based practices that support the routine delivery of vaccines should be part of all obstetrical practices. Vaccines need to be both recommended AND provided by those delivering obstetrical care in all practices settings. Curricula should be developed for trainees about the risks and benefits of immunization during pregnancy and postpartum, and vaccination competency should be an expected requirement of training programs for all obstetrical care providers. Access to
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vaccine registries by obstetrical providers is critical to being able to monitor an individual woman’s vaccination status as well as to measure the rates of vaccine coverage achieved by each obstetrical care practice. Missed opportunities for vaccination should be identified in this manner and feedback mechanisms implemented in order to improve the quality of the maternal immunization platform among individuals and practices. The movement to electronic medical records can facilitate this process and contribute to improved vaccination coverage. Issues regarding funding for maternal immunization programs should be addressed in each jurisdiction to ensure that access to vaccination during pregnancy is available to all women and that providers are compensated for the cost of delivering the vaccination program. Liability concerns need to be addressed for practitioners as well as for vaccine manufacturers, some of whom are still reluctant to undertake the necessary clinical trials to provide the safety and efficacy data which the public, providers, and regulators need in order to be comfortable with maternal immunization recommendations. These ongoing research needs must be met to support the recommendations and to inform their expansion to other disease targets. Understanding the mechanism of protection provided by maternal immunization, the duration of protection, the optimal timing of immunization during pregnancy, the need for repeat dosing in subsequent pregnancies, and the effect of maternal-derived antibodies on the active immune response in the newborn are just some of the information that is needed to support maternal immunization programs. As well, there is a critical need for implementation research to determine what interventions are effective in addressing the concerns of the public and healthcare providers, recognizing the diversity of stakeholders comprising even a single one of these groups. In summary, maternal immunization as a strategy to protect pregnant women, fetuses, and newborns will be most effective by establishing a formal maternal immunization platform similar to the infant and adolescent programs that have achieved remarkable successes (Figure 1). In order to have a significant impact on the disease burden on newborns, implementation of the strategy at national and international levels is needed, with leadership taken by each jurisdiction’s technical advisory group. This new platform must be integrated into the routine practice of all obstetrical care providers, through extensive education in training programs and ongoing continuing education programs. Communication to the public is essential, and understanding and addressing the concerns of pregnant women is fundamental to the success of the intervention. While a number of interventions have been studied, most strategies lack data supporting their effectiveness; the lack of evidence-based recommendations fuels doubt among both the public and providers and weakens the strength of vaccination recommendations. A coordinated strategy must be implemented in order to achieve high rates of maternal immunization coverage.
Methods The focus of this review was to provide an overview of the effect of knowledge, attitudes, and practices of pregnant women and their healthcare providers on improving uptake of vaccines that are recommended during pregnancy.
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Literature search We identified potentially eligible reports by searching the following databases on June 8, 2015: CINAHL, PubMed, Science Direct, Springer Link, ProQuest, Oxford Journals, Taylor and Francis, Wiley, and Google Scholar via the Web of Knowledge. Search terms were identified and then corroborated using the index of keywords for each database. Our search terms were “maternal vaccination," “maternal immunization (immunisation)," “vaccination," “immunization (immunisation)," “pregnancy," “uptake," “education," “attitudes," “promotion” and /or “interventions." The search was limited to articles published in English between 2005 and 2015. We also keyed the titles of relevant articles into the PubMed “related articles” feature to
identify similar reports and into the “times cited” feature in the Web of Knowledge. In addition, we completed a manual search by reviewing the reference lists of all included articles for additional studies. The initial inclusion criteria were articles in English involving vaccination during pregnancy. A relatively small range of research-based articles and reports were retrieved. In total, 95 citations using the search terms were identified from the following sources: CINAHL (5), PubMed (36), Science Direct (10), Springer Link (3), ProQuest (3), Oxford Journals (3), Taylor and Francis (4), Wiley (2), and Google Scholar via the Web of Knowledge (14), and manual search (15). Two reviewers (SAH and DMM) assessed the abstracts. A data collection form was used to abstract data from the studies independently. The form covered information about
Figure 1. Supports required for the establishment of a “maternal immunization platform.” HIC: High-income countries; LMIC: Low- and middle-income countries; RSV: Respiratory Syncytial Virus; Tdap: Tetanus, diphtheria, and acellular pertussis vaccine
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study design, setting, aim of the study, population studied, outcome measures, and important results that identified barriers, facilitators, and logistical information. The reviewers discussed any discrepancies in their results to reach agreement. Very few papers were identified that described intervention-based research (nD10). Both qualitative and quantitative studies including systematic reviews were included in this review. Thirty-one studies were eliminated because they focused on postpartum immunization rather than immunization during pregnancy. Sixty-four articles were eligible for inclusion, meeting our criteria which addressed our primary objective of describing the effect of knowledge, attitudes, and practices of pregnant women and their healthcare providers on improving the uptake of vaccines that are recommended during pregnancy. To be included, the study needed to specify the vaccine used, location, and population studied. We excluded studies that did not address factors that affected uptake of recommended vaccines during pregnancy and vaccine coverage rates. Duplicates were not extracted as well as papers that did not meet the inclusion criteria.
Disclosure of potential conflicts of interest No potential conflicts of interest were disclosed.
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