- Email: [email protected]
Barriers to influenza vaccination among pregnant women
Vaccine 31 (2013) 2874–2878
Contents lists available at SciVerse ScienceDirect
Vaccine journal homepage: www.elsevier.com/locate/vaccine
Barriers to influenza vaccination among pregnant women Catherine Eppes a,∗ , Alison Wu a , Whitney You b , K.A. Cameron a , Patricia Garcia a , William Grobman a a b
Northwestern University, Feinberg College of Medicine, 250 Superior Street, Suite 5-2175, Chicago, IL 60611, United States Naval Medical Center, 2450 Craven Street, Building 3300, Naval Base, San Diego, CA 92136, United States
a r t i c l e
i n f o
Article history: Received 26 December 2012 Received in revised form 4 April 2013 Accepted 11 April 2013 Available online 24 April 2013 Keywords: H1N1 Vaccine acceptance
a b s t r a c t Objective: Despite pregnant women’s increased morbidity and mortality from influenza, vaccination rates remain low. This study intended to evaluate barriers to pregnant women’s uptake of influenza vaccine. Study design: A survey was designed that assessed participant demographics, knowledge, beliefs, attitudes, and general experiences with seasonal and 2009 novel H1N1 influenza. Associations between patient characteristics and vaccine uptake were then assessed. Results: 88 women completed the survey. Women who correctly answered >75% of knowledge questions regarding influenza were significantly more likely to accept the influenza vaccine (seasonal: p = 0.04, H1N1: p < 0.01). Conversely, patients who declined the vaccine were more likely to hold false beliefs, such as perceiving that the vaccine was not protective (seasonal: p < 0.01, H1N1: p < .01) and that they were not at risk for influenza (seasonal: p < 0.01). Conclusion: The reasons for influenza vaccine declination in pregnant patients include lower levels of knowledge and unfavorable attitudes regarding the safety and efficacy of the vaccine, and suggest the importance of education as a tool to improve vaccination uptake © 2013 Elsevier Ltd. All rights reserved.
1. Introduction Pregnant women infected with influenza have increased morbidity and mortality compared to non-pregnant women, with correspondingly increased rates of hospitalization and ICU admission [1,2]. The recent 2009 H1N1 pandemic illustrated this susceptibility, with hospitalization rates in pregnant women being four times higher than those in the general population [2]. The influenza vaccine has been studied extensively in pregnant women. A large randomized controlled trial found it not only to be safe and effective, but also able to decrease the frequency of influenza like illness (ILI) [3] among neonates. Poehling et al. also found that maternal vaccination was associated with a reduced risk of influenza hospitalizations in infants less than 6 months old [4]. Influenza vaccination is not approved for infants less than 6 months of age. Thus, besides vaccination of household contacts, maternal vaccination resulting in transplacental transfer of antibodies is the only method of prevention in this age range. Based on the available data, both the CDC and ACOG recommend vaccination for all pregnant women. Despite this recommendation, historical vaccination rates have been reported to range from
∗ Corresponding author at: Baylor College of Medicine, One Baylor Plaza, Mail Stop 610, Houston, TX 77030, United States. Tel.: +1 713 873 8794. E-mail addresses: [email protected], [email protected] (C. Eppes). 0264-410X/$ – see front matter © 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.vaccine.2013.04.031
2% to 15% [5,6]. During the 2009 H1N1 influenza pandemic the overall rate of vaccination improved among pregnant women, but a substantial portion of these women continued to decline influenza vaccination [7,8]. The reasons for this continued high frequency of declination remains uncertain and poorly characterized. In this study we sought to determine which factors are associated with influenza vaccine uptake among pregnant women. 2. Methods This study was conducted from October 2009 until June 2010. Regarding the timing of this study, the CDC declared a pandemic state in June of 2009, with the H1N1 vaccine becoming available in September of 2009. Pregnant women were in the highest priority group to receive vaccination. From October 2009 to June 2010, 88 patients were enrolled, as a convenience sample, from outpatient and inpatient settings of an urban tertiary care medical center. Women cared for in the inpatient and outpatient offices included those covered by private and government insurance. Women in the outpatient clinics included those with both low-risk and high-risk obstetric conditions. Women were not eligible for the survey if they had an egg allergy or religious basis for declining vaccination. However, no patient who was approached met these exclusion criteria. Women who agreed to participate and signed informed consent then underwent an interview with one of three obstetricians (CE, AW, or WY)
C. Eppes et al. / Vaccine 31 (2013) 2874–2878
2875
Table 1 Patient demographics stratified by vaccine acceptance. Demographic
Seasonal vaccine Acceptor N = 59
Age (years) 18–25 26–30 31–35 36–40 >40 Race Asian Black White Hispanic Parity Nulliparous Parous Trimester First Second Third
P Decliner N = 26
H1N1 Vaccine
P
Acceptor N = 59
Decliner N = 29
12 (52) 18 (78) 16 (84) 11 (61) 2 (40)
11 (48) 5 (12) 3 (16) 7 (39) 3 (60)
5 (71) 16 (59) 25 (71) 12 (86)
2 (29) 11 (41) 10 (29) 2 (14)
21 (75) 38 (63)
7 (25) 22 (37)
1 (33) 17 (57) 39 (75)
2 (66) 13 (43) 13 (25)
0.53 15 (68) 16 (73) 14 (78) 12 (67) 2 (40)
7 (32) 6 (27) 4 (22) 6 (33) 3 (60)
4 (57) 16 (64) 28 (80) 9 (69)
3 (43) 9 (36) 7 (20) 4 (31)
18 (67) 40 (70)
9 (33) 17 (30)
1 (33) 17 (61) 40 (78)
2 (66) 11 (39) 11 (22)
0.08
0.52
0.37
0.75
0.26
0.17
0.17
All data presented as N (%). Note: As patient were allowed to decline certain questions, not all numbers add to 88.
who had been trained to administer the survey in a standard fashion. The interview consisted of an 88-question survey (see supplementary information) that assessed patient knowledge, attitudes, beliefs, and general experience with influenza. A woman’s demographic characteristics and health literacy also were assessed. This survey was composed of items from previous influenza-related studies in non-pregnant populations and piloted among pregnant women to assess clarity prior to patient enrollment [9]. The first portion of the questionnaire focused specifically on seasonal influenza, while the second portion contained the same questions but was focused on 2009 H1N1 influenza. Questions that probed the extent of a woman’s knowledge about influenza vaccination could be answered “true”, “false”, or “I don’t know”, and were considered to demonstrate lack of knowledge when a participant chose the answer that was incorrect or answered “I don’t know.” The overall knowledge score was calculated as the number of correct answers divided by the total number of knowledge questions. A score of greater than 75% was used as the primary comparison between groups to represent both an average level of knowledge and since it was the median percentage correct within the entire study population. Attitudes and belief questions were answered on a 4-point Likert scale (strongly agree, slightly agree, slightly disagree and strongly disagree). For the purposes of this analysis, categories were analyzed individually and as collapsed overall “agree” and “disagree” categories. Questions that probed a woman’s prior experience with and exposure to influenza and vaccination could be answered as “yes” or “no.” Women were asked both whether they received H1N1 vaccination, and whether they were planning to receive the H1N1 vaccine this year in order to discern if lack of immunization was related to vaccine availability. Participant characteristics assessed included age, self-identified race, medical history, gestational age at the time of the survey, type of obstetric care provider, number of children under 18 years of age in their household, and employment status. Literacy was assessed using the Rapid Estimate of Adult Literacy in Medicine (REALM), a validated 66-question health literacy test [11]. Statistical analysis was performed using SAS software (version 9.1, SAS Institute, Cary, NC). Categorical data were compared using 2 or the Fischer’s exact statistic as appropriate. A p value of <0.05 was considered statistically significant. Prior to its initiation, this study was approved by the Northwestern University institutional review board.
3. Results Of the 98 women who were asked to participate, 88 (90%) provided consent and performed the survey. Women in this study ranged from 18 to 45 years of age. Just over half were employed, 60% were insured with Medicaid, and 28.2% were cared for in “high-risk” obstetric clinics. The majority of patients were in either the second (34.1%) and third (62.2%) trimester of pregnancy. Of the women surveyed, 69% had received the seasonal vaccine and 67% had received the H1N1 vaccine. Acceptance of the seasonal vaccine was highly associated with acceptance of the H1N1 vaccine (p < 0.01). Characteristics of the population, stratified by vaccine acceptance, are presented in Table 1. Maternal age, race, gestational age, employment status, number of children in the household, and perception of their own health status, were not significantly related to vaccine uptake. Conversely, women were more likely to receive either vaccine if they were cared for in the high-risk clinic (seasonal: p = 0.01, H1N1: p = 0.03). While women were asked both whether they received H1N1 vaccination, and whether they were planning to receive the vaccine, there were no women who did not receive the vaccine but were planning to do so. Results from the remainder of the survey are presented in Tables 2–5. The mean knowledge score in the entire study for seasonal influenza was 74.4 ± 0.14%, and H1N1 69.5 ± 2%. Patients who received the vaccine had a higher mean score (seasonal: 77 ± 0.14%, H1N1: 75.8 ± 16%) while patients who declined the vaccine had lower mean scores (seasonal: 70 ± 0.12%, H1N1: 57.2 ± 21%). Patients who accepted the vaccines demonstrated significantly greater factual knowledge about the vaccine and influenza infection. For example, women who accepted vaccination were more likely to know that the vaccine cannot give someone the flu (H1N1 p < 0.01). Overall, women who accepted the vaccines were significantly more likely to correctly answer more than 75% of the knowledge questions. (seasonal p = 0.04 and H1N1 p < 0.01). The primary knowledge score of greater than the 75% percentile was utilized as this was the mean knowledge score overall for the seasonal vaccine. However, the distinction between vaccine decliners and acceptors remained significant for the seasonal vaccine for scores of greater than 80% (p = 0.03) and greater than 70% (p = 0.03), but not greater than 60% (p = 0.75). All score cutt-offs analyzed for H1N1 remained significant, i.e. greater than 90% (p = 0.06), through greater than 50% (p = 0.0001).
2876
C. Eppes et al. / Vaccine 31 (2013) 2874–2878
Table 2 Patient response to knowledge questions. Question
Response
Seasonal
Correct Incorrect Correct Incorrect Correct Incorrect Correct Incorrect Correct Incorrect Correct Incorrect Correct Incorrect Correct Incorrect Correct Incorrect Correct Incorrect Correct Incorrect Correct Incorrect <75% >75%
The seasonal flu is not contagious There is more than one type of flu The seasonal flu virus is the same every year People with the seasonal flu are never sick enough to be admitted to the hospital The seasonal flu is more dangerous for pregnant women than non-pregnant women The seasonal flu shot contains a live virus All pregnant women should get the seasonal flu shot The seasonal flu shot is not safe in pregnancy The seasonal flu shot is safe during breastfeeding The seasonal flu shot can give someone the flu When a pregnant women get the flu shot it helps protect her baby. . . The seasonal flu shot helps protect pregnant women against the flu General knowledge score
H1N1
Yes
No
p value
Yes
No
p value
55 4 51 8 46 12 58 1 51 8 37 22 51 8 54 3 31 28 30 29 39 20 58 1 34 25
26 0 20 6 21 5 25 1 25 1 21 5 13 13 19 7 12 14 10 16 20 6 24 2 21 5
0.17
58 1 31 28
28 1 19 10
0.60
58 1 56 3 35 24 51 8 57 2 30 29 38 21 43 16 58 1 19 40
27 2 27 2 23 6 14 15 17 12 10 19 6 23 17 12 23 6 20 9
0.28
0.29
0.79 0.55 0.18 0.1 <0.01 0.01 0.59 0.29 0.32 0.17 0.04
0.21 0.73 0.06 <0.01 <0.01 0.15 <0.01 0.18 <0.01 <0.01
*Note: Column Yes and No (in this table and all subsequent) refer to whether participants received vaccination for either seasonal influenza or 2009 H1N1. Table 3 Patient beliefs and attitudes regarding influenza. Question
Response
The flu will be a problem this year
Agree Disagree Agree Disagree Agree Disagree Agree Disagee Agree Disagree Agree Disagee Agree Disagee Agree Disagee Agree Disagee
I am at risk for the flu The flu can kill me The flu shot causes birth defects The flu shot is safe when a person is not pregnant I am afraid of what might be in the shot The flu shot prevents the flu The flu shot will protect me from getting the flu The flu shot does not work
Seasonal
H1N1
Yes
No
p value
Yes
No
p value
46 13 33 26 5 54 4 54 56 3 19 40 50 9 52 7 12 47
18 8 16 10 14 12 11 15 22 4 17 9 14 12 15 11 10 16
0.39
53 6 30 29 53 5 6 51 55 4 26 33 54 5 57 2 3 55
24 5 18 11 24 5 14 14 20 9 26 3 19 10 15 13 9 19
0.49
0.62 <0.01 <0.01 0.12 0.01 <0.01 <0.01 0.08
0.32 0.29 <0.01 0.01 <0.01 <0.01 <0.01 <0.01
Table 4 General experiences regarding influenza. Question
Response
Have you ever gotten the flu shot before In the 12 months before you were pregnant did you see the doctor? Did you doctor offer you the flu shot Did your doctor tell you about the flu Has anyone in your household had the flu? Have you ever had a reaction to the flu shot?
Yes No Yes No Yes No Yes No Yes No Yes No
Seasonal
H1N1
Yes
No
P
41 18 55 4 51 8 44 14 20 38 20 39
10 16 19 4 18 8 14 12 5 21 5 21
0.01
Yes
No
P
56 3 52 7 11 48
25 3 23 5 1 28
0.33
0.01 0.61 0.04 0.29 0.26
Note: H1N1 vaccine acceptors were not asked questions referring to receiving the shot before, as the vaccine was not available previously.
0.45 0.51
C. Eppes et al. / Vaccine 31 (2013) 2874–2878
2877
Table 5 Media exposure regarding influenza. Question
How closely have you been following the news? Thinking back in the past week, have you actively looked for info? In the last week, have you seen, read, or heard any stories about the seasonal flu?
Response
Very-somewhat close Not too or not at all YES NO YES NO
Vaccine acceptors also were significantly more likely to have different health beliefs than decliners. Vaccine acceptors were more likely to believe the flu could lead to their own death (seasonal p < 0.01). They were also more likely to believe the vaccine was effective and safe, answering that it would prevent the flu (seasonal p < 0.01) and was safe in pregnancy (seasonal p < 0.01). They were less likely to believe that the vaccines were dangerous, disagreeing with statements that the vaccination causes birth defects (seasonal p < 0.01, H1N1 p < 0.01). Also, they were more likely to have seen a physician in the year prior to their pregnancy (p = 0.01) and to have a physician who told them about the flu (p = 0.04). Interestingly, while 71.4% of H1N1 vaccine decliners responded that the vaccine is safe outside of pregnancy, they felt that the flu shot is not safe in pregnancy (p < 0.01). While both individual Likert scale values and collapsed “agreement” and “disagreement” categories were analyzed, the authors felt that total “agreement” or “disagreement” were the most relevant issues. The majority of analyses remained significant whether total “agreement” and “disagreement” categories or each individual Likert category were utilized. The only question that was significant for the collapsed categories and became non-significant when each individual Likert category was compared was “the flu can kill me” (seasonal p = 0.34). Regarding media and literacy, we found all patients reported using multiple media sources of information and were identified as having high levels of health literacy. 56.5% of patients reported using the Internet, 61.2% reported identified their physician as a source of information, and 58% reported utilizing friends and family as sources of information about influenza. The majority of participants were in the highest literacy group (85.8%). Neither the source of information (except for physician interaction) nor health literacy were significantly related to patient vaccination status. 4. Discussion In our study we found that a number of factors are associated with pregnant women’s declination of influenza vaccination. These factors include less influenza-related knowledge, less perception of their own risks from infection, and lack of belief in the safety and efficacy of the vaccine. Moreover, there was evidence of the key behavior-modifying role that health care providers can have. Those women who recalled specific discussions with a physician about influenza infection and the benefits of vaccination were significantly more likely to accept the vaccine. Media exposure, in contrast, appeared to be unrelated to vaccine uptake, as were demographic factors and literacy status. These findings are promising with regard to improving acceptance of influenza vaccination, as non-modifiable characteristics appeared least associated with vaccine uptake, while modifiable characteristics (e.g., knowledge, beliefs) and actions that may lead to changes in behavior (e.g., physician discussion) were significantly associated with higher vaccination frequency.
Seasonal
H1N1
Yes
No
p value
Yes
No
p value
32 27 4 55 15 46
18 8 4 22 2 24
0.2
49 10 7 52 13 46
22 7 4 25 4 24
0.42
0.21 0.15
0.8 0.25
Previous studies also have evaluated barriers to vaccination among pregnant women [8,12,13], although have often focused on just one of the domains that may be associated with vaccination. Fisher et al., for example, assessed 13 potential barriers to seasonal and H1N1 vaccination [8], and found that 25% of women reported declining vaccination because they did not know that vaccination was “important” for their health. They also found racial disparity in vaccination status, with black women accepting less vaccination than white and Hispanic women. Fabry assessed Canadian women in the framework of the health beliefs model, focusing on perceived susceptibility to H1N1 and severity of H1N1 [12]. They found exposure to official governmental websites, trust in health professionals’ advice, and belief in vaccine efficacy were associated with vaccination. Brownsyne et al. explored women’s intention to receive vaccination and found women with more self-risk perception and less distrust of the healthcare system were more likely to vaccinate [13]. Knowledge specifically was evaluated in a study by Yudin et al., who found pregnant women’s overall understanding of influenza was poor. Ninety percent of women were not aware that pregnancy carries a greater risk of ILI compared to non-pregnancy, approximately 50% were aware that the vaccine is safe during pregnancy and breast feeding, and 80% believed that the vaccine can cause birth defects [14]. Goldfarb found the main reason for vaccine acceptance was a desire for pregnant women to protect their baby, while the main reason for declination was fear of harm to self [7]. Our study differs from prior studies in that it explores the multiple domains (e.g., knowledge, health beliefs, health literacy) among a single population associated with potential vaccine acceptance. Because vaccine declination could arise from the interplay of numerous beliefs and barriers, assessing a multitude of domains is most likely to allow exploration of the many factors involved in declination. Limitations of our study include that it was performed during a time of an influenza pandemic, and therefore may not be applicable to other epochs. We also had a small number of participants with low or limited literacy, and therefore cannot adequately explore whether or not interactions with one’s literacy ability exist. Similarly, our study may be underpowered to detect small differences in other factors between vaccine acceptors and decliners. This study was conducted only one time per participant, therefore any patients that “crossed over”, or decided to accept vaccination at a later point in time were not re-assessed. Lastly, as this was a convenience sample, we cannot exclude the possibility of selection bias. In summary, vaccine declination was associated with less knowledge about influenza, lower perceived susceptibility, and beliefs that the vaccine is not efficacious or safe. Also, recall of information about influenza and vaccination provided by health professionals was associated with vaccination uptake, stressing the important role such professionals can have in their patients’ health behaviors. The results cumulatively emphasize the importance of accurate information dissemination, in particular regarding the safety and efficacy of the vaccines, which can be enhanced through provider-patient communication.
2878
C. Eppes et al. / Vaccine 31 (2013) 2874–2878
Acknowledgements The authors would like to acknowledge Stacy Bailey for her contributions regarding assistance with SNAP software. Conflicts of interest: The authors have no conflicts of interest to disclose. Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.vaccine. 2013.04.031. References [1] Dodds L, McNeil SA, Fell DB, Allen VM, Coombs A, Scott J, et al. Impact of influenza exposure on rates of hospital admissions and physician visits because of respiratory illness among pregnant women. CMAJ 2007;176(February (4)):463–8. [2] Jamieson DJ, Honein MA, Rasmussen SA, William JL, Swerdlow DL, Biggerstaff MS, et al. H1N1 2009 influenza virus infection during pregnancy in the USA. Lancet 2009;374(August (9688)):451–8. [3] 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(October (15)):1555–64.
[4] Poehling A, Szilagyi P, Staat M, Snively B, Payne D, Bridges C, et al. Impact of maternal immunization on influenza hospitalizations in infants. Am J Obstet Gynecol 2011;204(June (6 Suppl 1)):1–7. [5] Lu P, Bridges CB, Euler GL, Singleton JA. Influenza vaccination of recommended adult populations, U.S. 1989–2005. Vaccine 2008;26(14):1786–93. [6] Tamma PD, Ault KA, del Rio C, Steinhoff MC, Halsey NA, Omer SB. Safety of influenza vaccination during pregnancy. Am J Obstet Gynecol 2005;192(4):1098–106. [7] Goldfarb I, Panda B, Wylie B, Riley L. Uptake of influenza vaccine in pregnant women during the 2009 H1N1 influenza pandemic. Am J Obstet Gynecol 2011;204(June (6 Suppl 1)):S1–4. [8] Fisher B, Scott J, Hart J, Winn V, Gibbs R, Lynch A. Behaviors and perceptions regarding seasonal and H1N1 influenza vaccination during pregnancy. Am J Obstet Gynecol 2011;204(June (6 Suppl 1)):1–5. [9] Cameron KA, Kamanda-Kosseh M, Roloff ME, Baker DW, Makoul G. Increasing African American seniors’ knowledge, positive attitudes, and intention to be vaccinated against influenza through a multimedia education program. J Gen Intern Med 2009;24(Suppl. 1). S10. [11] Davis TC, Crouch MA, Long SW, Jackson RH, Bates P, George RB, et al. Rapid estimate of adult literacy in medicine: a shortened screening instrument. Fam Med 1991;23(August (6)):433–5. [12] Fabry P, Gagneur A, PAsquier JC. Determinants of A(H1N1) vaccination: crosssectional study of a population of pregnant women in Quebec. Vaccine 2011;29:1824–9. [13] Brownsyne M, Tucker E, Coleman J, Armstrong K, Shea J. Risk perceptions, worry, or distrust: what drives pregnant women’s decisions to accept the H1N1 vaccine? Matern Child Health J 2009, published online October. [14] Yudin MH, Salaripour M, Sgro MD. Pregnant women’s knowledge of influenza and the use and safety of the influenza vaccine during pregnancy. J Obstet Gynaecol Can 2009;31(February (2)):120–5.
Contents lists available at SciVerse ScienceDirect
Vaccine journal homepage: www.elsevier.com/locate/vaccine
Barriers to influenza vaccination among pregnant women Catherine Eppes a,∗ , Alison Wu a , Whitney You b , K.A. Cameron a , Patricia Garcia a , William Grobman a a b
Northwestern University, Feinberg College of Medicine, 250 Superior Street, Suite 5-2175, Chicago, IL 60611, United States Naval Medical Center, 2450 Craven Street, Building 3300, Naval Base, San Diego, CA 92136, United States
a r t i c l e
i n f o
Article history: Received 26 December 2012 Received in revised form 4 April 2013 Accepted 11 April 2013 Available online 24 April 2013 Keywords: H1N1 Vaccine acceptance
a b s t r a c t Objective: Despite pregnant women’s increased morbidity and mortality from influenza, vaccination rates remain low. This study intended to evaluate barriers to pregnant women’s uptake of influenza vaccine. Study design: A survey was designed that assessed participant demographics, knowledge, beliefs, attitudes, and general experiences with seasonal and 2009 novel H1N1 influenza. Associations between patient characteristics and vaccine uptake were then assessed. Results: 88 women completed the survey. Women who correctly answered >75% of knowledge questions regarding influenza were significantly more likely to accept the influenza vaccine (seasonal: p = 0.04, H1N1: p < 0.01). Conversely, patients who declined the vaccine were more likely to hold false beliefs, such as perceiving that the vaccine was not protective (seasonal: p < 0.01, H1N1: p < .01) and that they were not at risk for influenza (seasonal: p < 0.01). Conclusion: The reasons for influenza vaccine declination in pregnant patients include lower levels of knowledge and unfavorable attitudes regarding the safety and efficacy of the vaccine, and suggest the importance of education as a tool to improve vaccination uptake © 2013 Elsevier Ltd. All rights reserved.
1. Introduction Pregnant women infected with influenza have increased morbidity and mortality compared to non-pregnant women, with correspondingly increased rates of hospitalization and ICU admission [1,2]. The recent 2009 H1N1 pandemic illustrated this susceptibility, with hospitalization rates in pregnant women being four times higher than those in the general population [2]. The influenza vaccine has been studied extensively in pregnant women. A large randomized controlled trial found it not only to be safe and effective, but also able to decrease the frequency of influenza like illness (ILI) [3] among neonates. Poehling et al. also found that maternal vaccination was associated with a reduced risk of influenza hospitalizations in infants less than 6 months old [4]. Influenza vaccination is not approved for infants less than 6 months of age. Thus, besides vaccination of household contacts, maternal vaccination resulting in transplacental transfer of antibodies is the only method of prevention in this age range. Based on the available data, both the CDC and ACOG recommend vaccination for all pregnant women. Despite this recommendation, historical vaccination rates have been reported to range from
∗ Corresponding author at: Baylor College of Medicine, One Baylor Plaza, Mail Stop 610, Houston, TX 77030, United States. Tel.: +1 713 873 8794. E-mail addresses: [email protected], [email protected] (C. Eppes). 0264-410X/$ – see front matter © 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.vaccine.2013.04.031
2% to 15% [5,6]. During the 2009 H1N1 influenza pandemic the overall rate of vaccination improved among pregnant women, but a substantial portion of these women continued to decline influenza vaccination [7,8]. The reasons for this continued high frequency of declination remains uncertain and poorly characterized. In this study we sought to determine which factors are associated with influenza vaccine uptake among pregnant women. 2. Methods This study was conducted from October 2009 until June 2010. Regarding the timing of this study, the CDC declared a pandemic state in June of 2009, with the H1N1 vaccine becoming available in September of 2009. Pregnant women were in the highest priority group to receive vaccination. From October 2009 to June 2010, 88 patients were enrolled, as a convenience sample, from outpatient and inpatient settings of an urban tertiary care medical center. Women cared for in the inpatient and outpatient offices included those covered by private and government insurance. Women in the outpatient clinics included those with both low-risk and high-risk obstetric conditions. Women were not eligible for the survey if they had an egg allergy or religious basis for declining vaccination. However, no patient who was approached met these exclusion criteria. Women who agreed to participate and signed informed consent then underwent an interview with one of three obstetricians (CE, AW, or WY)
C. Eppes et al. / Vaccine 31 (2013) 2874–2878
2875
Table 1 Patient demographics stratified by vaccine acceptance. Demographic
Seasonal vaccine Acceptor N = 59
Age (years) 18–25 26–30 31–35 36–40 >40 Race Asian Black White Hispanic Parity Nulliparous Parous Trimester First Second Third
P Decliner N = 26
H1N1 Vaccine
P
Acceptor N = 59
Decliner N = 29
12 (52) 18 (78) 16 (84) 11 (61) 2 (40)
11 (48) 5 (12) 3 (16) 7 (39) 3 (60)
5 (71) 16 (59) 25 (71) 12 (86)
2 (29) 11 (41) 10 (29) 2 (14)
21 (75) 38 (63)
7 (25) 22 (37)
1 (33) 17 (57) 39 (75)
2 (66) 13 (43) 13 (25)
0.53 15 (68) 16 (73) 14 (78) 12 (67) 2 (40)
7 (32) 6 (27) 4 (22) 6 (33) 3 (60)
4 (57) 16 (64) 28 (80) 9 (69)
3 (43) 9 (36) 7 (20) 4 (31)
18 (67) 40 (70)
9 (33) 17 (30)
1 (33) 17 (61) 40 (78)
2 (66) 11 (39) 11 (22)
0.08
0.52
0.37
0.75
0.26
0.17
0.17
All data presented as N (%). Note: As patient were allowed to decline certain questions, not all numbers add to 88.
who had been trained to administer the survey in a standard fashion. The interview consisted of an 88-question survey (see supplementary information) that assessed patient knowledge, attitudes, beliefs, and general experience with influenza. A woman’s demographic characteristics and health literacy also were assessed. This survey was composed of items from previous influenza-related studies in non-pregnant populations and piloted among pregnant women to assess clarity prior to patient enrollment [9]. The first portion of the questionnaire focused specifically on seasonal influenza, while the second portion contained the same questions but was focused on 2009 H1N1 influenza. Questions that probed the extent of a woman’s knowledge about influenza vaccination could be answered “true”, “false”, or “I don’t know”, and were considered to demonstrate lack of knowledge when a participant chose the answer that was incorrect or answered “I don’t know.” The overall knowledge score was calculated as the number of correct answers divided by the total number of knowledge questions. A score of greater than 75% was used as the primary comparison between groups to represent both an average level of knowledge and since it was the median percentage correct within the entire study population. Attitudes and belief questions were answered on a 4-point Likert scale (strongly agree, slightly agree, slightly disagree and strongly disagree). For the purposes of this analysis, categories were analyzed individually and as collapsed overall “agree” and “disagree” categories. Questions that probed a woman’s prior experience with and exposure to influenza and vaccination could be answered as “yes” or “no.” Women were asked both whether they received H1N1 vaccination, and whether they were planning to receive the H1N1 vaccine this year in order to discern if lack of immunization was related to vaccine availability. Participant characteristics assessed included age, self-identified race, medical history, gestational age at the time of the survey, type of obstetric care provider, number of children under 18 years of age in their household, and employment status. Literacy was assessed using the Rapid Estimate of Adult Literacy in Medicine (REALM), a validated 66-question health literacy test [11]. Statistical analysis was performed using SAS software (version 9.1, SAS Institute, Cary, NC). Categorical data were compared using 2 or the Fischer’s exact statistic as appropriate. A p value of <0.05 was considered statistically significant. Prior to its initiation, this study was approved by the Northwestern University institutional review board.
3. Results Of the 98 women who were asked to participate, 88 (90%) provided consent and performed the survey. Women in this study ranged from 18 to 45 years of age. Just over half were employed, 60% were insured with Medicaid, and 28.2% were cared for in “high-risk” obstetric clinics. The majority of patients were in either the second (34.1%) and third (62.2%) trimester of pregnancy. Of the women surveyed, 69% had received the seasonal vaccine and 67% had received the H1N1 vaccine. Acceptance of the seasonal vaccine was highly associated with acceptance of the H1N1 vaccine (p < 0.01). Characteristics of the population, stratified by vaccine acceptance, are presented in Table 1. Maternal age, race, gestational age, employment status, number of children in the household, and perception of their own health status, were not significantly related to vaccine uptake. Conversely, women were more likely to receive either vaccine if they were cared for in the high-risk clinic (seasonal: p = 0.01, H1N1: p = 0.03). While women were asked both whether they received H1N1 vaccination, and whether they were planning to receive the vaccine, there were no women who did not receive the vaccine but were planning to do so. Results from the remainder of the survey are presented in Tables 2–5. The mean knowledge score in the entire study for seasonal influenza was 74.4 ± 0.14%, and H1N1 69.5 ± 2%. Patients who received the vaccine had a higher mean score (seasonal: 77 ± 0.14%, H1N1: 75.8 ± 16%) while patients who declined the vaccine had lower mean scores (seasonal: 70 ± 0.12%, H1N1: 57.2 ± 21%). Patients who accepted the vaccines demonstrated significantly greater factual knowledge about the vaccine and influenza infection. For example, women who accepted vaccination were more likely to know that the vaccine cannot give someone the flu (H1N1 p < 0.01). Overall, women who accepted the vaccines were significantly more likely to correctly answer more than 75% of the knowledge questions. (seasonal p = 0.04 and H1N1 p < 0.01). The primary knowledge score of greater than the 75% percentile was utilized as this was the mean knowledge score overall for the seasonal vaccine. However, the distinction between vaccine decliners and acceptors remained significant for the seasonal vaccine for scores of greater than 80% (p = 0.03) and greater than 70% (p = 0.03), but not greater than 60% (p = 0.75). All score cutt-offs analyzed for H1N1 remained significant, i.e. greater than 90% (p = 0.06), through greater than 50% (p = 0.0001).
2876
C. Eppes et al. / Vaccine 31 (2013) 2874–2878
Table 2 Patient response to knowledge questions. Question
Response
Seasonal
Correct Incorrect Correct Incorrect Correct Incorrect Correct Incorrect Correct Incorrect Correct Incorrect Correct Incorrect Correct Incorrect Correct Incorrect Correct Incorrect Correct Incorrect Correct Incorrect <75% >75%
The seasonal flu is not contagious There is more than one type of flu The seasonal flu virus is the same every year People with the seasonal flu are never sick enough to be admitted to the hospital The seasonal flu is more dangerous for pregnant women than non-pregnant women The seasonal flu shot contains a live virus All pregnant women should get the seasonal flu shot The seasonal flu shot is not safe in pregnancy The seasonal flu shot is safe during breastfeeding The seasonal flu shot can give someone the flu When a pregnant women get the flu shot it helps protect her baby. . . The seasonal flu shot helps protect pregnant women against the flu General knowledge score
H1N1
Yes
No
p value
Yes
No
p value
55 4 51 8 46 12 58 1 51 8 37 22 51 8 54 3 31 28 30 29 39 20 58 1 34 25
26 0 20 6 21 5 25 1 25 1 21 5 13 13 19 7 12 14 10 16 20 6 24 2 21 5
0.17
58 1 31 28
28 1 19 10
0.60
58 1 56 3 35 24 51 8 57 2 30 29 38 21 43 16 58 1 19 40
27 2 27 2 23 6 14 15 17 12 10 19 6 23 17 12 23 6 20 9
0.28
0.29
0.79 0.55 0.18 0.1 <0.01 0.01 0.59 0.29 0.32 0.17 0.04
0.21 0.73 0.06 <0.01 <0.01 0.15 <0.01 0.18 <0.01 <0.01
*Note: Column Yes and No (in this table and all subsequent) refer to whether participants received vaccination for either seasonal influenza or 2009 H1N1. Table 3 Patient beliefs and attitudes regarding influenza. Question
Response
The flu will be a problem this year
Agree Disagree Agree Disagree Agree Disagree Agree Disagee Agree Disagree Agree Disagee Agree Disagee Agree Disagee Agree Disagee
I am at risk for the flu The flu can kill me The flu shot causes birth defects The flu shot is safe when a person is not pregnant I am afraid of what might be in the shot The flu shot prevents the flu The flu shot will protect me from getting the flu The flu shot does not work
Seasonal
H1N1
Yes
No
p value
Yes
No
p value
46 13 33 26 5 54 4 54 56 3 19 40 50 9 52 7 12 47
18 8 16 10 14 12 11 15 22 4 17 9 14 12 15 11 10 16
0.39
53 6 30 29 53 5 6 51 55 4 26 33 54 5 57 2 3 55
24 5 18 11 24 5 14 14 20 9 26 3 19 10 15 13 9 19
0.49
0.62 <0.01 <0.01 0.12 0.01 <0.01 <0.01 0.08
0.32 0.29 <0.01 0.01 <0.01 <0.01 <0.01 <0.01
Table 4 General experiences regarding influenza. Question
Response
Have you ever gotten the flu shot before In the 12 months before you were pregnant did you see the doctor? Did you doctor offer you the flu shot Did your doctor tell you about the flu Has anyone in your household had the flu? Have you ever had a reaction to the flu shot?
Yes No Yes No Yes No Yes No Yes No Yes No
Seasonal
H1N1
Yes
No
P
41 18 55 4 51 8 44 14 20 38 20 39
10 16 19 4 18 8 14 12 5 21 5 21
0.01
Yes
No
P
56 3 52 7 11 48
25 3 23 5 1 28
0.33
0.01 0.61 0.04 0.29 0.26
Note: H1N1 vaccine acceptors were not asked questions referring to receiving the shot before, as the vaccine was not available previously.
0.45 0.51
C. Eppes et al. / Vaccine 31 (2013) 2874–2878
2877
Table 5 Media exposure regarding influenza. Question
How closely have you been following the news? Thinking back in the past week, have you actively looked for info? In the last week, have you seen, read, or heard any stories about the seasonal flu?
Response
Very-somewhat close Not too or not at all YES NO YES NO
Vaccine acceptors also were significantly more likely to have different health beliefs than decliners. Vaccine acceptors were more likely to believe the flu could lead to their own death (seasonal p < 0.01). They were also more likely to believe the vaccine was effective and safe, answering that it would prevent the flu (seasonal p < 0.01) and was safe in pregnancy (seasonal p < 0.01). They were less likely to believe that the vaccines were dangerous, disagreeing with statements that the vaccination causes birth defects (seasonal p < 0.01, H1N1 p < 0.01). Also, they were more likely to have seen a physician in the year prior to their pregnancy (p = 0.01) and to have a physician who told them about the flu (p = 0.04). Interestingly, while 71.4% of H1N1 vaccine decliners responded that the vaccine is safe outside of pregnancy, they felt that the flu shot is not safe in pregnancy (p < 0.01). While both individual Likert scale values and collapsed “agreement” and “disagreement” categories were analyzed, the authors felt that total “agreement” or “disagreement” were the most relevant issues. The majority of analyses remained significant whether total “agreement” and “disagreement” categories or each individual Likert category were utilized. The only question that was significant for the collapsed categories and became non-significant when each individual Likert category was compared was “the flu can kill me” (seasonal p = 0.34). Regarding media and literacy, we found all patients reported using multiple media sources of information and were identified as having high levels of health literacy. 56.5% of patients reported using the Internet, 61.2% reported identified their physician as a source of information, and 58% reported utilizing friends and family as sources of information about influenza. The majority of participants were in the highest literacy group (85.8%). Neither the source of information (except for physician interaction) nor health literacy were significantly related to patient vaccination status. 4. Discussion In our study we found that a number of factors are associated with pregnant women’s declination of influenza vaccination. These factors include less influenza-related knowledge, less perception of their own risks from infection, and lack of belief in the safety and efficacy of the vaccine. Moreover, there was evidence of the key behavior-modifying role that health care providers can have. Those women who recalled specific discussions with a physician about influenza infection and the benefits of vaccination were significantly more likely to accept the vaccine. Media exposure, in contrast, appeared to be unrelated to vaccine uptake, as were demographic factors and literacy status. These findings are promising with regard to improving acceptance of influenza vaccination, as non-modifiable characteristics appeared least associated with vaccine uptake, while modifiable characteristics (e.g., knowledge, beliefs) and actions that may lead to changes in behavior (e.g., physician discussion) were significantly associated with higher vaccination frequency.
Seasonal
H1N1
Yes
No
p value
Yes
No
p value
32 27 4 55 15 46
18 8 4 22 2 24
0.2
49 10 7 52 13 46
22 7 4 25 4 24
0.42
0.21 0.15
0.8 0.25
Previous studies also have evaluated barriers to vaccination among pregnant women [8,12,13], although have often focused on just one of the domains that may be associated with vaccination. Fisher et al., for example, assessed 13 potential barriers to seasonal and H1N1 vaccination [8], and found that 25% of women reported declining vaccination because they did not know that vaccination was “important” for their health. They also found racial disparity in vaccination status, with black women accepting less vaccination than white and Hispanic women. Fabry assessed Canadian women in the framework of the health beliefs model, focusing on perceived susceptibility to H1N1 and severity of H1N1 [12]. They found exposure to official governmental websites, trust in health professionals’ advice, and belief in vaccine efficacy were associated with vaccination. Brownsyne et al. explored women’s intention to receive vaccination and found women with more self-risk perception and less distrust of the healthcare system were more likely to vaccinate [13]. Knowledge specifically was evaluated in a study by Yudin et al., who found pregnant women’s overall understanding of influenza was poor. Ninety percent of women were not aware that pregnancy carries a greater risk of ILI compared to non-pregnancy, approximately 50% were aware that the vaccine is safe during pregnancy and breast feeding, and 80% believed that the vaccine can cause birth defects [14]. Goldfarb found the main reason for vaccine acceptance was a desire for pregnant women to protect their baby, while the main reason for declination was fear of harm to self [7]. Our study differs from prior studies in that it explores the multiple domains (e.g., knowledge, health beliefs, health literacy) among a single population associated with potential vaccine acceptance. Because vaccine declination could arise from the interplay of numerous beliefs and barriers, assessing a multitude of domains is most likely to allow exploration of the many factors involved in declination. Limitations of our study include that it was performed during a time of an influenza pandemic, and therefore may not be applicable to other epochs. We also had a small number of participants with low or limited literacy, and therefore cannot adequately explore whether or not interactions with one’s literacy ability exist. Similarly, our study may be underpowered to detect small differences in other factors between vaccine acceptors and decliners. This study was conducted only one time per participant, therefore any patients that “crossed over”, or decided to accept vaccination at a later point in time were not re-assessed. Lastly, as this was a convenience sample, we cannot exclude the possibility of selection bias. In summary, vaccine declination was associated with less knowledge about influenza, lower perceived susceptibility, and beliefs that the vaccine is not efficacious or safe. Also, recall of information about influenza and vaccination provided by health professionals was associated with vaccination uptake, stressing the important role such professionals can have in their patients’ health behaviors. The results cumulatively emphasize the importance of accurate information dissemination, in particular regarding the safety and efficacy of the vaccines, which can be enhanced through provider-patient communication.
2878
C. Eppes et al. / Vaccine 31 (2013) 2874–2878
Acknowledgements The authors would like to acknowledge Stacy Bailey for her contributions regarding assistance with SNAP software. Conflicts of interest: The authors have no conflicts of interest to disclose. Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.vaccine. 2013.04.031. References [1] Dodds L, McNeil SA, Fell DB, Allen VM, Coombs A, Scott J, et al. Impact of influenza exposure on rates of hospital admissions and physician visits because of respiratory illness among pregnant women. CMAJ 2007;176(February (4)):463–8. [2] Jamieson DJ, Honein MA, Rasmussen SA, William JL, Swerdlow DL, Biggerstaff MS, et al. H1N1 2009 influenza virus infection during pregnancy in the USA. Lancet 2009;374(August (9688)):451–8. [3] 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(October (15)):1555–64.
[4] Poehling A, Szilagyi P, Staat M, Snively B, Payne D, Bridges C, et al. Impact of maternal immunization on influenza hospitalizations in infants. Am J Obstet Gynecol 2011;204(June (6 Suppl 1)):1–7. [5] Lu P, Bridges CB, Euler GL, Singleton JA. Influenza vaccination of recommended adult populations, U.S. 1989–2005. Vaccine 2008;26(14):1786–93. [6] Tamma PD, Ault KA, del Rio C, Steinhoff MC, Halsey NA, Omer SB. Safety of influenza vaccination during pregnancy. Am J Obstet Gynecol 2005;192(4):1098–106. [7] Goldfarb I, Panda B, Wylie B, Riley L. Uptake of influenza vaccine in pregnant women during the 2009 H1N1 influenza pandemic. Am J Obstet Gynecol 2011;204(June (6 Suppl 1)):S1–4. [8] Fisher B, Scott J, Hart J, Winn V, Gibbs R, Lynch A. Behaviors and perceptions regarding seasonal and H1N1 influenza vaccination during pregnancy. Am J Obstet Gynecol 2011;204(June (6 Suppl 1)):1–5. [9] Cameron KA, Kamanda-Kosseh M, Roloff ME, Baker DW, Makoul G. Increasing African American seniors’ knowledge, positive attitudes, and intention to be vaccinated against influenza through a multimedia education program. J Gen Intern Med 2009;24(Suppl. 1). S10. [11] Davis TC, Crouch MA, Long SW, Jackson RH, Bates P, George RB, et al. Rapid estimate of adult literacy in medicine: a shortened screening instrument. Fam Med 1991;23(August (6)):433–5. [12] Fabry P, Gagneur A, PAsquier JC. Determinants of A(H1N1) vaccination: crosssectional study of a population of pregnant women in Quebec. Vaccine 2011;29:1824–9. [13] Brownsyne M, Tucker E, Coleman J, Armstrong K, Shea J. Risk perceptions, worry, or distrust: what drives pregnant women’s decisions to accept the H1N1 vaccine? Matern Child Health J 2009, published online October. [14] Yudin MH, Salaripour M, Sgro MD. Pregnant women’s knowledge of influenza and the use and safety of the influenza vaccine during pregnancy. J Obstet Gynaecol Can 2009;31(February (2)):120–5.