Seasonal influenza data and data from the 2009 H1N1 and previous influenza pandemics1–6 show that pregnant women are at increased risk for morbidity and death from influenza. To reduce the risk for seasonal influenza among pregnant women, the Advisory Committee on Immunization Practices and the American College of Obstetricians and Gynecologists recommend that all women who are pregnant or expect to be pregnant during the influenza season should be vaccinated with the trivalent inactivated influenza vaccine.7,8 In addition to protecting pregnant women, influenza vaccination during pregnancy has been shown to decrease the risk for influenza among infants up to 6 months of age9 Because influenza vaccine is not recommended for use among infants younger than 6 months of age, maternal immunization during pregnancy is thus an important strategy for preventing infection in these infants.7 However, despite these recommendations and evidence of the protective effects of seasonal influenza vaccines, vaccine coverage among pregnant women in the United States remains low. Recent data from the National Health Interview Survey show that, for the United States, rates of seasonal influenza vaccination coverage among pregnant women ranged from 12.3% during the 2005 to 2006 influenza season to 24.2% during the 2007 to 2008 season.5,7,10,11
Low vaccination coverage rates imply that there may be barriers to seasonal influenza vaccination among pregnant women. Previous study results have shown that factors affecting pregnant women's decisions about whether to get a seasonal influenza vaccination include their knowledge about the vaccines and their perceptions of the vaccines' safety, whether their health care providers advised them to get vaccinated or offered to vaccinate them, and the extent of their health care providers' knowledge about the risks of influenza during pregnancy.16–21 Recent estimates based on data from the Pregnancy Risk Assessment and Monitoring System and from the National Health Interview Survey showed that seasonal influenza vaccine coverage varies by state and has increased for pregnant women since the 2005 influenza season but still remains low compared with other priority groups.10,18 Our purpose in conducting this study among Pregnancy Risk Assessment and Monitoring System participants in Georgia and Rhode Island was to identify facilitators of and barriers to pregnant women being vaccinated against seasonal influenza by identifying demographic, service use, and lifestyle factors associated with influenza vaccination during pregnancy among women who had recently given birth to a live infant.
MATERIALS AND METHODS
To identify correlates of influenza vaccine coverage among pregnant women, we analyzed population-based data from Pregnancy Risk Assessment and Monitoring System, an ongoing, population-based surveillance system that collects data on a wide range of maternal behaviors and experiences before, during, and after pregnancy. In collaboration with the Centers for Disease Control and Prevention, 37 states and New York City currently administer Pregnancy Risk Assessment and Monitoring System surveys. The primary mode of Pregnancy Risk Assessment and Monitoring System data collection is a mail survey, and nonresponders are contacted by telephone. Each month, participating jurisdictions mail questionnaires to a stratified random sample of 100–300 women who, according to birth certificate data, gave birth to a live neonate in the previous 2–6 months. All participating jurisdictions use a core questionnaire, but they can also add questions from a set of standard modules, one of which includes questions about use of the seasonal influenza vaccine. We analyzed data from two states, Rhode Island (n=2,732) and Georgia (n=2,692), whose Pregnancy Risk Assessment and Monitoring System questionnaires included the influenza module in 2006 and 2007. To obtain a study sample large enough for us to perform multivariable analyses and identify correlates of seasonal influenza vaccine coverage by state, we pooled data for 2006 and 2007, the 2 most recent years for which Pregnancy Risk Assessment and Monitoring System data were available. The Pregnancy Risk Assessment and Monitoring System project was approved by the Centers for Disease Control and Prevention's Institutional Review Board.
Variables examined included seasonal influenza vaccination coverage among women during their most recent pregnancy, demographic and service use indicators, and several chronic disease-related risk factors. Response rates for the survey were 70% or greater for both years in both states. Both states' surveys included the question, “Did you get a flu vaccination during your most recent pregnancy?” The Rhode Island survey asked about health care provider offer or encouragement: “At any time during your pregnancy, did a doctor, nurse, or other health care worker offer you a flu vaccination or tell you to get one?” The Georgia survey did not include a question on health care provider offer or encouragement but the survey asked the following question: “What were your reasons for not getting a flu vaccination during your most recent pregnancy? For each item, circle Y (yes) if it was a reason for you and circle N (no) if it was not a reason or did not apply to you.” The reasons offered as options were: “My doctor didn't mention anything about a flu vaccination during my pregnancy”; “I was worried about the side effects of the flu vaccination for me”; “I was worried that the flu vaccination might harm my baby”; “I wasn't pregnant during the flu season”; “I was in my first trimester during the flu season”; “I don't normally get a flu vaccination”; and “Other” (followed by a blank space for women to write in their responses). Demographic variables considered in the analysis were maternal race and ethnicity (non-Hispanic African American, non-Hispanic white, Hispanic, other); maternal age at delivery (younger than 20, 20–24, 25–29, 30–34, 35 years or older), marital status (married, other), maternal education (less than high school, high school, more than high school), parity at the time of the survey (primipara, multipara), Medicaid payment for prenatal care (yes or no), and timing of prenatal care in (first trimester, later). Other variables we considered were cigarette smoking (yes or no), body mass index (less than 30 kg/m2, 30 or greater), and history of chronic or pregnancy-induced hypertension and diabetes (yes or no for each). These demographic, service use, and behavioral variables were available for both states.
Women who did not answer the question regarding receipt of seasonal influenza vaccination (n=156 for Georgia and n=94 for Rhode Island) were excluded from our analyses as were those who did not provide data for other variables; rates of missing data for specific variables ranged from less than 1% to 6%. To produce estimates applicable to the total population of women in each state who had recently delivered a liveborn neonate, we used SUDAAN software to account for the complex sampling design of the Pregnancy Risk Assessment and Monitoring System survey. Weighting adjusts for nonresponses of survey participants and noncoverage weights correct for discrepancy between sampling frame and actual number of births. To identify correlates of vaccine receipt, we conducted both bivariable and multivariable logistic analyses. Variables included in the models were those that previous study results showed to be associated with seasonal influenza vaccination among pregnant women as well as demographic and service use variables. We also examined the comments from participants in the Georgia survey about their reasons for not getting the seasonal influenza vaccine. Of the 244 comments written on the survey, 242 were legible. Examination of these comments indicated that approximately 70% could be classified into new categories and the rest could either be assigned to existing categories or were too idiosyncratic to be categorized.
The results of our analysis indicated that the percentage of women reporting that they received seasonal influenza vaccination during their most recent pregnancy was 18.4% (95% confidence interval [CI]: 15.9–21.1) in Georgia and 31.9% (95% CI 29.8–34.0) in Rhode Island. Results of bivariable analyses of Georgia data showed that non-Hispanic African-American women were less likely to have received the seasonal influenza vaccine than were non-Hispanic white women (Table 1). However, in multivariable analyses, only parity was significantly associated with vaccine receipt (adjusted odds ratio [OR] 0.60; 95% CI 0.40–0.89) (Table 1).
Results of bivariable analyses of Rhode Island data showed that Hispanic women as well as those who did not smoke were more likely than non-Hispanic whites or those who smoked to have received the seasonal influenza vaccine and that women who were not married and those whose prenatal care was not paid for by Medicaid were less likely to have received the vaccine than were their counterparts. Overall, in Rhode Island, 32% (95% CI 29.9–34.0) of the women received offer or encouragement from their health care providers and 68% (95% CI 65.9–70.1) did not report receiving offer or encouragement. Women who reported that their health care providers encouraged or offered them to be vaccinated were more likely to have received the vaccine than women whose health care providers did not (65% compared with 4%, respectively) (Table 2). Multivariable analyses results, however, showed health care–provider encouragement (adjusted OR 56.62; 95% CI 37.43–85.63) and not smoking to be significantly associated with vaccine receipt (adjusted OR 1.92; 95% CI 1.25–2.94).
Among pregnant women in Georgia who did not get vaccinated, the most common reasons given for not doing so were that their physician did not encourage them and that they normally did not get the seasonal influenza vaccination (Table 3). Approximately 6% of women selected “other” and wrote in reasons for not being vaccinated other than the options presented on the survey questionnaire. Approximately one-third of the written-in reasons overlapped with the categories provided in the question itself and the rest or approximately 70% of these reasons were different from the options provided in the survey. Of the women who cited actual “other” reasons for not being vaccinated, 24% indicated that no vaccine was available or that there was a vaccine shortage at the facility where they went to get immunized; 13% cited concerns about the safety of the influenza vaccine and their belief that not enough was known about vaccine administration to pregnant women (eg, “No research about flu shot and pregnancy”); 12% mentioned that their health care providers discouraged them from being vaccinated (eg, “Dr. said I was healthy,” “didn't need one,” and “my MD felt that it was not necessary”); 10% indicated that they did not like shots; 7% said they had been vaccinated before their pregnancy; and 5% reported being allergic to eggs.
Our results showed that seasonal influenza vaccination coverage among pregnant women and the correlates of that coverage varied by state, but the two states also asked different questions. In Georgia, the major correlate of vaccine receipt was parity; primiparas were more likely to have received the vaccine than were multiparas, perhaps reflecting multiple demands and commitments experienced by women with children. In Rhode Island, health care–provider encouragement to be vaccinated was strongly associated with vaccine receipt among pregnant women; the magnitude of this association was similar to that observed in a study by Tong et al.17 This association, which has also been shown by the results of other studies,12–16 suggest that health care providers can play a significant role in increasing influenza vaccination coverage rates among pregnant women both by advising women to be vaccinated at any time during their pregnancy and by addressing women's concerns about being vaccinated during prenatal care visits. However, more than 40% of Georgia women who were not vaccinated during their pregnancy indicated that their physician did not mention influenza vaccination to them while they were pregnant. This suggests that many health care providers may need to be educated about the risk for severe influenza complications among pregnant women, the importance of influenza vaccine to prevent these complications, and the need for women to be counseled accordingly. The need for such education has been noted previously.14,21,22 The concern that many of the Georgia Pregnancy Risk Assessment and Monitoring System participants reported having about lack of information concerning the safety of the influenza vaccine highlights the importance of communicating the risks and benefits of seasonal influenza vaccination, which has been noted previously.14,21,22
Factors that may prevent health care providers from recommending or offering influenza vaccinations to pregnant women include lack of facilities for vaccination storage and the belief that pregnant women should not be vaccinated,12,13,15 factors that previous studies have shown need to be addressed to facilitate optimal interaction between health care providers and their pregnant patients.12–17 Previous researchers have also called for vaccinations of pregnant women to be incorporated into the routine practices of obstetricians17 and to recommend specific strategies such as implementation of standing orders for seasonal influenza vaccination of pregnant women.23 A Rhode Island program, Immunize for Life, has been working to increase influenza vaccine availability to health care providers and to educate health care providers about the importance of vaccinating high-risk populations, including pregnant women. As part of this program, the Rhode Island Health Department is required to purchase influenza vaccine and distribute it to health care providers enrolled in the program.24 This program appears to have been effective in increasing rates of seasonal influenza vaccination among pregnant women.18,24 The results of our analyses may be useful to such programs by helping them identify women who might benefit from additional education or outreach strategies focusing on prevention such as those who have previously given birth and those who smoke.
Each year, more than four million births occur in the United States.25 Pregnancy Risk Assessment and Monitoring System data on influenza vaccination coverage, the effects of health care provider advice, and women's perceived barriers to vaccination may provide insights about ways to educate women concerning the importance of seasonal influenza vaccination and to encourage health care providers to counsel pregnant women to be vaccinated. Many women and health care providers may not be aware that, in 2004, both the Advisory Committee on Immunization Practices and the American College of Obstetricians and Gynecologists changed their recommendations concerning the administration of seasonal influenza vaccine to pregnant women from administration only during the second or third trimester to administration at any time during pregnancy.7 Approximately 25% of Georgia Pregnancy Risk Assessment and Monitoring System participants cited being in their first trimester as a reason for not getting the influenza vaccine, and others cited concerns about the safety of the influenza vaccine for pregnant women; both of these responses indicate a need to better communicate current vaccination recommendations to pregnant women and their health care providers. In short, despite evidence from numerous studies that seasonal influenza vaccines are safe for use by pregnant women,22 some pregnant women as well as their health care providers remain concerned about the safety of these vaccines.15–17
Findings of this study should be interpreted within the framework of the following limitations. First, because our analyses were based on Pregnancy Risk Assessment and Monitoring System data from only two states, our results are not generalizable to all pregnant women in the United States. In addition, only the Rhode Island Pregnancy Risk Assessment and Monitoring System survey asked participants whether their health care providers encouraged them to be vaccinated, and only the Georgia survey asked women who were not vaccinated about their reasons for not getting the vaccine. Second, Pregnancy Risk Assessment and Monitoring System data are based on self-reports by women 2–6 months postpartum and therefore may be affected by inaccurate recollections of survey participants. Third, the survey information about health care providers' recommendations was not confirmed by reports from health care providers; however, this was perhaps a rather minor limitation given that study results have shown a high correlation between health care providers' and patients' recollections of health care providers' recommendations.26,27 Despite these limitations, our findings provide insights into influenza vaccination coverage among pregnant women, barriers to their vaccination, and potential channels for improving coverage.
Data from the Pregnancy Risk Assessment and Monitoring System are used to provide state-specific estimates of influenza vaccination coverage of pregnant women, which are important for developing state-specific prevention and mitigation strategies. Findings from our analysis of Pregnancy Risk Assessment and Monitoring System survey data from Rhode Island and Georgia indicate a need for both physicians and pregnant women to be better educated1–8,19,20 regarding women's risk for influenza complications during pregnancy and the protective effects of influenza vaccination for women and their infants. Health care providers need to more consistently recommend influenza vaccination to their pregnant patients and to address women's concerns about vaccination during pregnancy ensuring that pregnant women understand the importance of getting immunized.
1.Jamieson DJ, Honein MA, Rasmussen SA, Williams JL, Swerdlow DL, Biggerstaff MS, et al. H1N1 2009 influenza virus infection during pregnancy in the USA. Lancet 2009;374:451–8.
2.Cox S, Posner SF, McPheeters M, Jamieson DJ, Kourtis AP, Meikle S. Hospitalizations with respiratory illness among pregnant women during influenza season. Obstet Gynecol 2006;107:1315–22.
3.Neuzil KM, Reed GW, Mitchel EF, Simonsen L, Griffin MR. Impact of influenza on acute cardiopulmonary hospitalizations in pregnant women. Am J Epidemiol 1998;148:1094–102.
4.Rasmussen SA, Jamieson DJ, Bresee JS. Pandemic influenza and pregnant women. Emerg Infect Dis 2008;14:95–100.
5.Naleway AL, Smith WJ, Mullooly JP. Delivering influenza vaccine to pregnant women. Epidemiol Rev 2006;28:47–53.
6.Harris JW. Influenza occurring in pregnant women: a statistical study of thirteen hundred and fifty cases. JAMA 1919;72:978–80.
7.Fiore AE, Shay DK, Broder K, Iskander JK, Uyeki TM, Mootrey G, et al. Prevention and control of influenza: recommendations of the Advisory Committee on Immunization Practices (ACIP), 2008. MMWR Recomm Rep 2008;57:1–60.
8.Influenza vaccination and treatment during pregnancy. ACOG Committee Opinion Number 305. American College of Obstetricians and Gynecologists. Obstet Gynecol 2004;104:1125–6.
9.Zaman K, Roy E, Arifeen SE, Rahman M, Raqib R, Wilson E, et al. Effectiveness of maternal influenza immunization in mothers and infants. N Engl J Med 2008;359:1555–64.
11.Lu P, Bridges CB, Euler GL, Singleton JA. Influenza vaccination of recommended adult populations, US, 1989–2005. Vaccine 2008;26:1786–93.
12.Centers for Disease Control and Prevention (CDC). Influenza vaccination in pregnancy: practices among obstetrician– gynecologists—United States, 2003–2004 influenza season. MMWR Morb Mortal Wkly Rep 2005;54:1050–2.
13.Silverman NS, Greif A. Influenza vaccination during pregnancy: patients' and physicians' attitudes. J Reprod Med 2001;46:989–94.
14.Munoz FM, Greisinger AJ, Wehmanene OA, Mouzoon M, Hoyle JC, Smith FA, et al. Safety of influenza vaccination during pregnancy. Am J Obstet Gynecol 2005;192:1098–106.
15.Esposito S, Tremolati E, Bellasio M, Chiarelli G, Marchisio P, Tiso B, et al. Attitudes and knowledge regarding influenza vaccination among hospital health workers caring for women and children. Vaccine 2007;25:5283–9.
16.Schrag SJ, Fiore AE, Gonik B, Reef S, Malik T, Singleton JA, et al. Vaccination and perinatal infection prevention practices among obstetrician–gynecologists. Obstet Gynecol 2003;101:704–10.
17.Tong A, Biringer A, Ofner-Agostini M, Upshur R, McGeer A. A cross-sectional study of maternity care providers' and women's knowledge, attitudes, and behaviours towards influenza vaccination during pregnancy. J Obstet Gynaecol Can 2008;30:404–10.
18.Centers for Disease Control and Prevention (CDC). Receipt of influenza vaccine during pregnancy among women with live births—Georgia and Rhode Island, 2004–2007. MMWR Morb Mortal Wkly Rep 2009;58:972–5.
19.Widelock D, Csizmas L, Klein S. Influenza, pregnancy, and fetal outcomes. Public Health Rep 1963;78:1–11.
20.Freeman DW, Barno A. Deaths from Asian influenza associated with pregnancy. Am J Obstet Gynecol 1959;78:1172–5.
21.Brewer NT, Hallman WK. Subjective and objective risk as predictors of influenza vaccination during the vaccine shortage of 2004–2005. Clin Infect Dis 2006;43:1379–86.
22.Tamma PD, Ault KA, del Rio C, Steinhoff MC, Halsey NA, Omer SB. Safety of influenza vaccination during pregnancy. Am J Obstet Gynecol 2009;201:547–52.
23.Mouzoon ME, Munoz FM, Greisinger AJ, Brehm BJ, Wehmanen OA, Smith FA, et al. Improving influenza immunization in pregnant women and healthcare workers. Am J Manag Care 2010;16:209–16.
25.Tejada-Vera B, Sutton PD. Births, marriages, divorces, and deaths: provisional data for April 2009. National Vital Statistics Reports 2009;58:1–13.
26.Sciamanna CN, Goldsten MG, Marcus BH, Lawrence K, Pinto BM. Accuracy of recall of exercise counseling among primary care patients. Prev Med 2004;39:1063–7.
27.Pbert L, Adams A, Quirk M, Hebert JR, Ockene JK, Luippold RS. The patient exit interviews as an assessment of physician-delivered smoking intervention: a validation study. Health Psychol 1999;18:183–8.