June 18th, 2018

Volume 54
June 2009
Number 6
Acceptance of a Pandemic Avian Influenza Vaccine in Pregnancy

Richard H. Beigi, M.D., M.Sc., Galen E. Switzer, Ph.D., and Leslie A. Meyn, M.S.


OBJECTIVE: To evaluate acceptance of a pandemic avian influenza vaccine among obstetric patients and nonphysician obstetric office personnel.
STUDY DESIGN: Two separate office-based questionnaires were administered to patients and nonphysician personnel. Questions included demographics, vaccine beliefs and acceptance of a potential pandemic avian influenza vaccine in pregnancy.
RESULTS: Questionnaires were completed by 394 of 600 (65.7%) eligible patients and 101 of 134 (75.3%) eligible office personnel. Only 15.4% of the patients stated they would definitely accept a pandemic influenza vaccine in pregnancy despite most (68%) reporting they would first consult their obstetrician for information. Fifty percent of the office personnel would not recommend a pandemic influenza vaccine to pregnant women and 40% reported unwillingness to accept the same vaccine if they were pregnant.
CONCLUSION: Barriers exist that may hinder mass vaccination efforts among the pregnant population during the next influenza pandemic. Preemptive educational efforts may assist in the acceptance of a pandemic vaccine among pregnant women and enable obstetricians to better provide disease prevention during the next influenza pandemic. (J Reprod Med 2009;54:341–346)

Keywords: avian influenza, pandemics, pregnancy, vaccination.

  Significant barriers may exist among
pregnant women and obstetric office
personnel that may complicate the
effectiveness of wide-scale mass
vaccination efforts for pandemic
influenza mitigation.

Disproportionate morbidity and mortality were recorded among pregnant women during the 20th-century influenza pandemics.1-5 In addition, numerous reports document increases in morbidity and hospitalization for cardiopulmonary complications in pregnancy during seasonal influenza epidemics.6-11 The most severe modern influenza pandemic was the 1918–19 “Spanish flu” pandemic, which killed roughly 30–50 million people worldwide and >500,000 in the United States.12 The emergence of H5N1 avian influenza in 1997, in addition to nearly 40 years transpiring since the last influenza pandemic, makes the threat of another severe pandemic similar to the Spanish flu a realistic possibility in the near future.13 In response to this emerging threat, wide-scale mitigation strategies have been proposed and are being developed. A cornerstone of these efforts includes the use of mass societal vaccination against the influenza strain responsible for the pandemic.
    The Advisory Committee on Immunization Practices and the American College of Obstetrics and Gynecology recognize this increased susceptibility to poor outcomes among influenza-infected pregnant women. Thus, both organizations recommend yearly influenza vaccination for all women who are or will be pregnant (in all trimesters) during influenza season, given the documented efficacy and safety of the trivalent inactivated vaccine.1,11 Despite these recommendations, a recent Centers for Disease Control and Prevention survey highlighted poor rates of national vaccination during pregnancy, noting that only 13% of obstetric patients were vaccinated during the 2003 influenza season.1,14 Thus, significant barriers to seasonal vaccination exist among this vulnerable patient population.
    The combination of the realistic threat of pandemic avian influenza, the previously documented disproportionate pandemic influenza–associated morbidity and mortality among pregnant women and the current poor national rates of seasonal influenza vaccination during pregnancy makes this a critical issue to preemptively address. Recognition of barriers to effective mass vaccination programs among pregnant women would provide useful information to target with educational efforts and would augment ongoing perinatal pandemic planning at all levels. The aim of the current study was to investigate attitudinal barriers and acceptance of a pandemic avian influenza vaccine among both obstetric patients and nonphysician obstetric office personnel.
Two anonymous questionnaires were constructed using formats for nonhypothesis testing survey research. The obstetric clinics at Magee-Womens Hospital of the University of Pittsburgh Medical Center (including resident-staffed and faculty clinics) were targeted for survey distribution. The first questionnaire was administered to current obstetric patients over a 5-month period (February–June 2007). The total targeted enrollment over that time period was 600. All women were asked to complete the anonymous questionnaire before their prenatal visits, and those who did had a colored label placed on their charts to avoid duplicate collection of questionnaire data. The second questionnaire was administered to the nonphysician employees in the same offices over the same time period who had direct patient contact (including nurses, patient care assistants, receptionists and clinical nursing leadership). These nonphysician employees were contacted at regular office business meetings and asked to complete the questionnaire. The office personnel eligible for participation were 134.
    Both questionnaires included items assessing demographics, beliefs about vaccination during pregnancy and questions regarding avian influenza (“bird flu”) vaccine acceptability. The specific questions for patients and personnel regarding bird flu were, respectively, (1) “Would you accept a bird flu vaccine during pregnancy if your prenatal care provider recommended it, even if it had never been tested in pregnancy?” (2) “If there was an outbreak of bird flu, would you recommend giving a vaccine to a pregnant woman even if it had not been tested in pregnancy?” and (3) “Would you take the same bird flu vaccine if you were pregnant?” In addition, pregnant women were asked whom they would contact first for information on pandemic influenza in the event of a pandemic. The phrases addressing the lack of testing of such a vaccine in pregnancy were chosen to approximate reality given the fact that it is highly unlikely that such a vaccine would have been previously tested among pregnant women prior to mass societal use in response to an influenza pandemic. Both questionnaires were evaluated and approved for use by the University of Pittsburgh Institutional Review Board. In addition, the questionnaires were pilot tested at Magee-Womens Hospital for comprehension, content and applicability by multiple volunteers and found to be unanimously acceptable.
    Sample size for the patient questionnaire was estimated given consideration of what would constitute a representative sample for a survey the goals of which were primarily descriptive. Collation and analysis of the data was performed using SPSS 14.0.1 statistical software (SPSS Inc., Chicago, Illinois). The data were summarized using frequencies and percents. Associations between demographic characteristics and vaccine acceptance were evaluated using Pearson’s 2 or Fisher’s exact test, where appropriate.
The response rate for the office personnel was 75.2% (101/134). Most participants were Caucasian (90.1%), with the remainder African American. One third of the respondents were nurses (33.7%), 34.7% were medical assistants, 23.8% were receptionists and the remainder clinical administrators. Nearly half (48.5%) had worked for <5 years, and 60.4% did not currently give vaccines to patients (Table I).

    Of the office personnel, greater than two thirds answered positively and reported (Table II): They believed vaccines prevented infectious diseases, that they receive the yearly influenza vaccine, they believed pregnant women were at an increased risk from influenza and that they would accept an annual influenza vaccine during their own pregnancy. However, when the office personnel were asked specifically about avian influenza (bird flu) and a potential influenza pandemic, more than half (50.5%) indicated that they would not recommend a pandemic influenza vaccine to pregnant women. In addition, roughly 40% (40.6%) reported that they themselves would not accept the same vaccine if they were pregnant. Various demographic factors, including ethnicity; job-related factors, including current administration of vaccines to patients; and their own seasonal influenza vaccine acceptance were evaluated for the relation to pandemic vaccine acceptance. There were no factors that were found to be related to or predictive of willingness to accept a potential pandemic influenza vaccine in pregnancy among the office personnel (p>0.05 for all factors, data not shown). This lack of relationship between background demographics/beliefs and pandemic vaccine acceptance was noted despite the fact that higher-educated employees, Caucasian employees and those who receive the yearly influenza vaccine were more likely to possess appropriate knowledge and to accept the seasonal influenza vaccine (p<0.05 for all, data not shown).

    Questionnaire response rate among obstetric patients was 394 of 600 (65.7%). Demographic characteristics of the responders match the overall demographics of the obstetric community served by the clinics involved and are noted in Table III. In the event of an influenza pandemic, 69.8% of responding pregnant women reported that they would seek medical information first from their obstetrician, 8.1% would consult their primary care provider, and 2.5% would consult the health department. The remainder responded with a combination of the above 3 choices, stated another source or did not respond to the question. When the combination answers were accounted for, 83.8% of the responses included the obstetrician, emphasizing the importance of the obstetrician’s input.

    When subsequently asked about their willingness to accept a bird flu vaccine during a pandemic, 15.7% of respondents stated yes, 44.7% stated they were unsure, and 37.1 responded no (Table IV). Multiple demographic factors were evaluated for a relationship to pandemic vaccine acceptability. Interestingly, younger age and nonwhite race were associated with increased seasonal influenza vaccine acceptability (p<0.02). However, no factors (including age, race or acceptance of vaccines for their own children) were found to be associated with pandemic influenza vaccine acceptability among the pregnant women, even when the analyses were stratified according to seasonal influenza vaccine acceptance (p>0.1 for all factors).
These data highlight potential conceptual and functional barriers to mass societal vaccination programs against a pandemic influenza strain that exist among obstetric patients and obstetric office personnel. Importantly, only 15.4% of patients stated they would definitely accept a pandemic avian influenza vaccine during pregnancy if it had not been tested in pregnancy. Moreover, greater than half of the office personnel would not recommend the same vaccine to the pregnant women during prenatal care visits, and approximately 40% would not themselves accept the same vaccine if they were pregnant. The wording of the questions, including the reference to the issue of nontesting of the vaccine in pregnancy, is relevant given the likely rapid production of such a vaccine. It is highly unlikely that there will be large-scale formal testing of such a vaccine before widespread societal use (and certainly no formal testing will be conducted on pregnant women). Importantly, the identified reluctance to accept such a vaccine among the obstetric community may complicate mass vaccination strategies during an impending influenza pandemic among this vulnerable patient population.
    These findings are of interest and concern given the amount of resources and attention being directed towards the production of a vaccine effective against the H5N1 avian influenza. Although such a vaccine, if successfully produced, holds tremendous promise for society as a whole in the face of an influenza pandemic, broad acceptance is required for high levels of societal benefit. Moreover, much awaited and necessary ethical guidance documents on resource and vaccine allocation during biologic disasters are beginning to appear in the literature and from the federal government.15-17 These guidance documents, while critical and vitally important to the greater public health, are structured on the premise that members of the population will accept such a vaccine if given the opportunity to receive it. The current paper suggests that the approach of mass vaccination may entail more forethought in terms of public acceptance if it is to reach its highest disease prevention potential. To date the studies that have been conducted with candidate H5N1 pandemic vaccines have demonstrated high levels of safety but only modest efficacy.18 Future research will hopefully improve on efficacy while simultaneously maintaining a high level of safety.
    The Centers for Disease Control and Prevention in 2003 reported data regarding seasonal influenza vaccination coverage among pregnant women.14 The investigation noted that only 13% of eligible pregnant women actually received influenza vaccinations during the 2003–04 influenza season despite formal recommendations for vaccination during pregnancy.1,11 There are many potential reasons for this low uptake of seasonal influenza vaccination in pregnancy, including providers not offering the vaccine in their offices and lack of an appreciation of the risk of influenza in pregnancy by providers.19,20 However, patient reluctance to accept vaccines in pregnancy is likely also a contributing factor to the low national uptake.19 The general reluctance to accept vaccines in pregnancy due to safety concerns appears legitimate from the consumer perspective despite scientific literature documenting the safety of the inactivated influenza vaccine in pregnancy.1,21 
    Nonphysician obstetric office personnel were included in this investigation given the amount of time spent between patients and such employees and the potential for their attitudes and beliefs to be transmitted to patients. While the exact impact of employees beliefs upon patients is unclear, data of concern were recently published addressing maternal and child health-care inpatient workers’ knowledge base. Esposito et al noted a poor knowledge base regarding the need for influenza vaccination in pregnancy and failure of these same health-care workers to make a recommendation to vaccinate this vulnerable patient population.22 It is highly conceivable that public hysteria would ensue during the next influenza pandemic, and an educated workforce would be critical in controlling the hysteria. Therefore, delineating beliefs and preemptively educating nonphysician medical personnel may prove to be an important component of effectively implementing large-scale public health endeavors such as mass vaccination. It is not clear why over two thirds of office personnel reported they would accept a seasonal influenza vaccine during their own pregnancy but less than half would accept a pandemic vaccine. The wording used regarding “untested in pregnancy” may be one possible explanation.
    An additional finding worth note suggests that obstetricians will play a central role in terms of providing accurate information to pregnant women during the next influenza pandemic. More than three quarters of pregnant women responded that their first contact for medical guidance during an influenza pandemic would include their obstetricians. This strongly emphasizes the need for focused efforts targeting practicing obstetricians and facilities providing maternity care regarding the safety and efficacy of influenza vaccination in pregnancy, pandemic influenza in general and pandemic influenza mitigation strategies.
    There are some limitations to the current investigation that warrant consideration. Primarily, this was a single-site investigation of employee and patient attitudes that may not be completely representative of the entire population. Despite the potential lack of generalizability, the data herein offer insight into the concerns pregnant women and obstetric personnel have regarding vaccination in pregnancy. It is acknowledged that the choice to use the phrase “untested in pregnancy” might have influenced respondents negatively. However, this is likely to be the reality of the situation that patients will face in this scenario, and thus it was chosen to approximate the decision process in the face of a mass vaccination program. The current questionnaire was anonymous, and no data were collected among nonresponders, introducing potential bias. However, the demographic profile among the pregnant participants closely resembles the background rates in the same practice setting, thus minimizing but not eliminating the potential for bias in terms of patient selection. It is also unclear if the low rates of vaccine acceptability noted during interpandemic periods reflect behavior that would occur during a true influenza pandemic. The concerns noted in these questionnaires may overestimate the level of reluctance to accept a rapidly developed pandemic avian influenza vaccine. However, the issue of reluctance will likely be apparent at some level and may hinder the true effectiveness of mass vaccination approaches in this and other susceptible populations.
    Despite these limitations, it appears that significant barriers may exist among pregnant women and obstetric office personnel that may complicate the effectiveness of wide-scale mass vaccination efforts for pandemic influenza mitigation. While it is currently unclear what attitudes underlie these barriers and if these attitudes would change when faced with a real influenza pandemic, proactive educational efforts have potential to overcome these barriers for this vulnerable patient population. Moreover, obstetricians will play a key role in terms of education of patients and care provision for the vulnerable patient population of pregnant women when the next influenza pandemic occurs. Thus, planning is warranted among providers of prenatal care and all facilities providing maternity services.
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From the Department of Obstetrics, Gynecology and Reproductive Sciences, Division of Reproductive Infectious Diseases, Magee-Womens Hospital of the University of Pittsburgh Medical Center; Departments of Medicine and Psychiatry, University of Pittsburgh School of Medicine; and Center for Health Equity and Promotion, VA Pittsburgh Healthcare System; and Magee-Womens Research Institute, Pittsburgh, Pennsylvania.

Presented in abstract form at the Infectious Diseases Society for Obstetrics and Gynecology Annual Clinical Meeting, Boston, August 9–11, 2007.

Address correspondence to: Richard H. Beigi, M.D., M.Sc., Department of Obstetrics, Gynecology and Reproductive Sciences, Magee-Womens Hospital of the University of Pittsburgh Medical Center, 300 Halket Street, Pittsburgh, PA 15213 (rbeigi@mail.magee.edu).

Financial Disclosure: The authors have no connection to any companies or products mentioned in this article.

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