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Contents lists available at ScienceDirect
Vaccine journal homepage: www.elsevier.com/locate/vaccine
Cross-sectional study on factors associated with influenza vaccine uptake and pertussis vaccination status among pregnant women in Germany
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Birte Bödeker a,b,∗ , Dietmar Walter a , Sabine Reiter a , Ole Wichmann a a b
Immunization Unit, Robert Koch Institute, Seestraße 10, 13353 Berlin, Germany Charité – University Medicine Berlin, Augustenburger Platz 1, 13353 Berlin, Germany
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Article history: Received 5 December 2013 Received in revised form 7 May 2014 Accepted 2 June 2014 Available online xxx
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Keywords: Pregnancy Influenza Pertussis Vaccination Attitude Knowledge
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1. Introduction
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Pregnant women and their newborns are at increased risk for influenza-related complications; the latter also have an increased risk for pertussis-related complications. In Germany, seasonal influenza vaccination is recommended for pregnant women since 2010. A dose of pertussis-containing vaccine has been recommended since 2004 for women of childbearing age if they have not been vaccinated within the past 10 years. We conducted a nationwide cross-sectional survey among pregnant women in February/March 2013 to assess knowledge, attitudes, and practices related to influenza vaccination during pregnancy and to identify factors associated with their pertussis vaccination status. In total, 1025 pregnant women participated and provided information through a self-administered questionnaire. Of these, 23.2% were vaccinated against seasonal influenza during the 2012/13 season; 15.9% during their pregnancy. Major reasons for being unvaccinated (n = 686 respondents) were lack of confidence in the vaccine (60.4%) and the perception that vaccination was not necessary (40.3%). Influenza vaccination during pregnancy was independently associated with having received influenza vaccine in the previous season, having received a recommendation from a physician, a high level of vaccine-related knowledge and of perceived disease severity. In contrast, knowledge of the recommendation for regular hand-washing to prevent influenza and the perception that vaccine-related side effects were likely to occur or likely to be severe were negatively associated with vaccine uptake. Receipt of a pertussis vaccine in the past 10 years was reported by 22.5% of participants. Pertussis vaccine uptake was independently associated with living in the Eastern federal states and receiving seasonal influenza vaccination annually, while a migration background was associated with a lower uptake. To enhance vaccine uptake in pregnant women and women of childbearing age, special efforts must be undertaken to improve knowledge of both recommendations and the benefits of vaccination. Gynecologists could serve as important facilitators. © 2014 Published by Elsevier Ltd.
Both pregnant women and newborns are at increased risk for influenza-related complications and hospitalization [1–3]. Influenza during pregnancy can cause stillbirth, preterm delivery, and growth retardation in the child [4,5]. Studies have demonstrated that influenza vaccination during pregnancy is safe and can effectively prevent influenza illness in pregnant women and also their newborns [6–9]. For these reasons, the World Health
∗ Corresponding author at: Immunization Unit, Robert Koch Institute, Seestrasse 10, 13353 Berlin, Germany. Tel.: +49 30 18754 3215; fax: +49 30 18754 3533. E-mail address: [email protected] (B. Bödeker).
Organization declared pregnant women as a group to be targeted by seasonal influenza vaccination with highest priority [10]. Despite compelling evidence on the safety and benefits of influenza vaccination during pregnancy, data from industrialized countries suggest only a low to moderate vaccine uptake in this target-group [11,12]. In Germany, seasonal influenza vaccination was recommended in August 2010 for all pregnant women from the 2nd trimester and for pregnant women with underlying chronic disease from the 1st trimester [13]. However, in the absence of an immunization registry no data on the vaccine uptake in this target-group is available thus far. In Germany, antenatal care is based on a nationwide standardized program for all pregnant women that is fully funded by health insurances and provided by office-based gynecologists, midwives and maternity clinics. Primary prenatal care including
http://dx.doi.org/10.1016/j.vaccine.2014.06.007 0264-410X/© 2014 Published by Elsevier Ltd.
Please cite this article in press as: Bödeker B, et al. Cross-sectional study on factors associated with influenza vaccine uptake and pertussis vaccination status among pregnant women in Germany. Vaccine (2014), http://dx.doi.org/10.1016/j.vaccine.2014.06.007
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pregnancy-related vaccination is primarily provided by officebased gynecologists [14]. Knowledge on the perceptions of pregnant women regarding influenza and on barriers and promoters for their decision to receive influenza vaccine are crucial to design tailored communication strategies and to increase vaccination coverage. Some studies reported on barriers such as vaccine safety concerns, mistrust in the vaccine, low risk perception of the disease, and poor vaccinerelated knowledge [15–18]. However, several of these studies had limitations due to their study design and small sample size, and knowledge/attitude among pregnant women may considerably vary from country to country. Similar to influenza, pertussis infection is associated with an increased risk for complications in infants when compared to other age-groups [19,20]. Since 2004, the German Standing Committee on Vaccination (STIKO) recommends pertussis vaccination for women of childbearing age as well for all close contacts of infants who have not received a pertussis vaccination within the past 10 years (so-called cocooning strategy). If a pregnant woman is not vaccinated before conception, STIKO recommends vaccination preferably in the first days after the birth of the child [21]. In contrast to the US or the United Kingdom, pertussis vaccination of pregnant women is currently not recommended in Germany [22,23]. We conducted a nationwide cross-sectional study among pregnant women aged 18 years and older living in Germany to assess influenza vaccine uptake during the 2012/13 season and pertussis vaccine uptake in the previous 10 years. In particular we aimed to assess knowledge of and attitudes towards seasonal influenza vaccination in this target-group.
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2. Methods
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2.1. Study design and population
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We conducted a nationwide cross-sectional survey among pregnant women between February and March 2013. The interviews were conducted by USUMA GmbH, a professional market and research company. Pregnant women were recruited based on a special sampling frame designed as an area sample (ADMSampling-System for Face-to-Face Surveys), which allows the assembly of representative samples for Germany [24]. Inclusion criteria for study participation were (i) being at least 18 years of age, (ii) being at least 12 weeks pregnant, and (iii) having a good command of the German language as assessed by study assistants responsible for the recruitment and data collection process in an area. Women were recruited in different ways: either (i) direct outreach, whereby pregnant women were invited to participate by our study assistants at specific sampling points in places where pregnant women typically congregate (e.g. gynecologist’s office, midwife’s office, maternity clinic), (ii) distribution of information leaflets by study assistants in these places inviting women to contact them by phone if interested in participating, or (iii) asking women to inform other pregnant women about the study. To obtain a study sample approximately representative for factors relevant to the study question, recruitment procedures included the use of quota proportions for specific population characteristics (age, educational status, and nationality) that were previously associated with vaccination against seasonal or pandemic influenza in the general population in Germany [25–27]. For this purpose, at the beginning of the survey study assistants were provided with quotas derived from different datasets gathered by the Federal Statistical Office of Germany to be met during recruitment. Since no representative perinatal dataset was available for Germany, quotas were based on data of mothers’ average age at the time of giving
birth, on educational level of women of childbearing age, and on nationality of newborns and their parents, respectively. All interested pregnant women were informed about the background, the objectives and the data protection and privacy related to this study. After providing verbal consent, participating women completed an anonymous, self-administered questionnaire that they returned directly to the study assistant. Participants did not receive any incentives. The institutional data protection officer of the Robert Koch Institute approved the study protocol; since no personal or clinical data were collected during the survey, an approval by the German Federal Commissioner for Data Protection and Freedom of Information was not required. 2.2. Study questionnaire and definitions The questionnaire elicited socio-economic and demographic data as well as information on knowledge, attitudes, and behavior regarding seasonal influenza vaccination and the disease, information needs concerning influenza vaccination, pertussis vaccination status, as well as women’s health status. Some of the sociodemographic items were used in previous surveys (such as the GEDA [28]), but were adapted to our setting. Further survey items were developed by reviewing the international literature. We applied single-item scales to the majority of items. Before study implementation, the questionnaire was pretested and subsequently modified. To assess the influenza vaccination status for season 2012/13, we asked whether the women had been vaccinated since 1st September 2012 and whether this was during or before their pregnancy. Furthermore, we asked for any pertussis vaccination within the last 10 years. We assessed disease- and vaccination-related knowledge of influenza. For this purpose, participants were asked to give their level of agreement with different statements that were answered on a 4-point Likert scale supplemented with the option of “don’t know”. Under the assumption that both incorrect as well as lack of knowledge reflect a lack of awareness for the importance of obtaining vaccination, we collapsed responses into two categories “agreed/disagreed correctly” vs. “agreed/disagreed incorrectly”, in which “don’t know” was assigned to “incorrect”. Vaccination-related questions were summed to obtain a knowledge score (range 0–4). We tested the scale’s internal consistency and excluded one item to obtain a final Cronbachs ∝ of 0.7. Based on the distribution of quartiles, the range of vaccination knowledge score was divided into four levels of knowledge. Migration background was defined as described by Schenk et al. on the basis of parents’ country of birth [29]. 2.3. Data analysis To control for possible selection biases, weighting factors were constructed. Since results of previous studies demonstrated that in Germany both age and place of residence were associated with influenza vaccine uptake in the general population [25,30], and since the above-mentioned quotas were not always fully met and did not take into account region-specific differences, we used the number of live births per federal state and per mother’s year of birth to calculate respective weighting factors. These factors were created on the basis of population data gathered by the Federal Statistical Office of Germany for 2011 [31]. Statistical analysis was performed using StataSE12 (StataCorp LP, College Station, Texas, US) using complex survey methods. Univariate and multivariate logistic regression analysis was applied to determine a potential association between influenza vaccine uptake during pregnancy and demographic characteristics, health-relevant factors, as well as attitude and knowledge. Odds ratios (OR) and 95% confidence intervals (CI) were calculated. Statistical significance was accorded when p < 0.05. All variables
Please cite this article in press as: Bödeker B, et al. Cross-sectional study on factors associated with influenza vaccine uptake and pertussis vaccination status among pregnant women in Germany. Vaccine (2014), http://dx.doi.org/10.1016/j.vaccine.2014.06.007
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identified in univariate analysis to be potentially associated with influenza vaccination (p-value 0.1 from the model. We then performed adjusted Wald test for independent variables with 0.05 ≤ p ≤ 0.1 to review whether these parameters create a statistically significant improvement in the fit of the model. Due to multicollinearity we removed two variables (perceived probability and severity of side effects for the unborn child after vaccination) which supplied redundant information. We proceeded analogously to assess potential associations of pertussis vaccination in the last 10 years with demographic and health behavior factors.
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3.1. Sample characteristics
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In total, 1030 pregnant women completed the survey questionnaire. Due to missing compliance with inclusion criteria five datasets were eliminated, resulting in 1025 datasets included in the final analysis. An overview of the characteristics of the study population in comparison to the general female population aged 18–49 years is provided in Table 1. The median age of women was 31 years (range 18–46) and 20.4% had a migration background. Approximately 60% of women were in the 2nd trimester of pregnancy and half were pregnant with their first child. 3.2. Influenza vaccination coverage and reasons for not being immunized During the 2012/13 season, 23.2% (95% CI: 20.6–26.0; crude without weighting: 23.4%) of pregnant women were vaccinated against seasonal influenza, whereas 15.9% (95% CI: 13.7–18.4; crude: 16.1%) received the flu shot while being pregnant. Reasons provided by the women for not being vaccinated are shown in Table 2. Among those not vaccinated and not intending to get vaccinated, more than half (60.4%) stated mistrusting the vaccine and 40.3% thought that vaccination was not necessary for them. Among those who mistrusted the vaccine, nearly two thirds (64.4%) reported fear of side effects. 3.3. Information seeking behavior regarding influenza vaccination Of all participating women, 40.5% actively sought information on influenza vaccination during pregnancy. Of these, most stated their physicians as an important information source (76.6%), followed by print media (59.7%), internet (47.6%) and relatives or friends (45%) (Fig. 1). Fig. 2 depicts the vaccination knowledge score of participants according to whether they utilized a specific information source or not. Results suggest that women who used the internet or television/radio had on average a slightly lower vaccination knowledge score compared to women seeking advice from other sources. In contrast, participants who sought advice from physicians or used print media had a significantly higher knowledge score than those who did not mention these sources. Participants who sought advice from physicians were also more often vaccinated than those who did not (39.6% vs. 7.8%, p < 0.001). There was no such association with any of the other utilized information sources. Of all participating women, 35.2% (95% CI: 32.2–38.4) reported a need for further information. Participants were particularly interested in receiving further information on vaccine-related side effects for pregnant women (78.2%) and their unborn child (73.2%) as well as on benefits for both the unborn child (76.2%) and
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Table 1 Characteristics of the study population and the general female population aged 18–49 years living in Germany in 2011. Study population, % (95% confidence)a Age-group (n = 1023) 18–24 years 25–29 years 30–34 years 35–39 years 40–49 years Country of birth (n = 1025) Germany Other country Migration background (n = 1025) Yes No Place of residence (n = 1025) Eastern Federal Statesc Western Federal States Highest educationd (n = 1025) Low Middle High Cannot be assigned Employment (n = 1021) Not employed Part-time employed Full-time employed Irregular employed Temporary suspended Monthly household income (n = 1008) ≤1500 D 1501–2000 D 2001–2500 D 2501–3000 D ≥3001 D Don’t know Family status (n = 1022) Married Civil union Single Other First pregnancy (n = 1020) Yes No Pregnancy trimester (n = 1025) Second Third
Genereral female population, % (n = 17,165,000)b
14.1 (12.3–16.1) 27.4 (24.8–30.2) 34.3 (31.2–37.6) 18.8 (16.3–21.7) 5.3 (3.8–7.3)
19.0 14.2 14.1 14.1 38.6
84.6 (82.1–86.8) 15.4 (13.2–17.9)
81.8 18.2
20.4 (17.9–23.2) 79.6 (76.8–82.1)
22.3 77.7
15.2 (13.1–17.4) 84.8 (82.6–86.9)
14.5 85.5
23.4 (20.8–26.3) 38.5 (35.4–41.7) 36.9 (33.8–40.2) 1.1 (0.6–2.0)
25.7 37.0 37.0 0.3
19.5 (17.1–22.2) 23.5 (20.7–26.4) 44.6 (41.4–47.8) 5.9 (4.5–7.6) 6.6 (5.1–8.5)
26.0 74.0e
13.3 (11.3–15.5) 13.1 (11.1–15.4) 20.8 (18.3–23.6) 23.7 (21.0–26.7) 23.4 (20.7–26.5) 5.7 (4.3–7.5)
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65.0 (61.9–68.0) 5.4 (4.1–7.0) 26.0 (23.3–28.8) 3.7 (2.6–5.1)
48.0 0.1 43.6 8.4
49.6 (46.3–52.8) 50.5 (47.2–53.7)
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62.0 (58.8–65.2) 38.0 (34.9–41.2)
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Weighted data (totals are not weighted). Data from the Federal Statistical Office of Germany [53]. c Brandenburg, Mecklenburg-Vorpommern, Saxony, Saxony-Anhalt, Thuringia. d Low: 9 years or less of school education, middle: at least 10 years of school education, high: university entrance diploma. e Includes all employed women including full-time, part-time or irregular employment as well as women who were temporary suspended b
the expectant mother (66.2%). Additional information regarding influenza-related complications during pregnancy was desired by 70.8%. Women who wished to obtain more information preferred to receive these from their gynecologists (89.2%), followed by general practitioners (50.4%) and print media (42.7%). Only one quarter of women (26.7%) mentioned the internet as desirable information source. 3.4. Factors associated with influenza vaccine uptake Results from univariate and multivariate logistic regression analysis on factors potentially associated with influenza vaccine
Please cite this article in press as: Bödeker B, et al. Cross-sectional study on factors associated with influenza vaccine uptake and pertussis vaccination status among pregnant women in Germany. Vaccine (2014), http://dx.doi.org/10.1016/j.vaccine.2014.06.007
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Midwife
Physician
Family and friends
Television and radio
Internet
Informational event
Print media
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Proportion [%] Fig. 1. Information sources utilized by pregnant women (n = 413) in Germany to obtain information about influenza vaccination during pregnancy. Footnote: weighted data; multiple answers were allowed.
Table 2 Reasons against seasonal influenza vaccination stated by 686 unvaccinated pregnant women, Germany, 2012/13. Reasons against influenza vaccinationa
Study population, % (95% confidence)b
I dont’t trust the vaccine. . . . . . becausec . . . Fear of side-effects Family members or friends had bad experiences with influenza vaccination. . . Media discussions around vaccine safety concerned me Vaccine is not effective Vaccine isn’t tested sufficiently Other In past, I had bad experiences with influenza vaccination Vaccination is not necessary for me I don’t know that pregnant women should be vaccinated In general, I am opposed to vaccination Somebody advised me not to get vaccinated Vaccine was not offered by my physician Fear of needles Due to organisational issues/vaccination was too time-consuming Vaccine was not available at the doctor’s office
60.4 (56.5–64.3)
a
64.4 (59.3–69.2) 32.9 (28.2–37.9)
uptake are shown in Table 3. Influenza vaccine uptake in 2012/13 was independently associated with influenza vaccination in the previous season, with a vaccination recommendation from a physician, a high vaccination knowledge score, and the degree of perceived disease severity. In addition, knowledge of the recommendation for regular hand-washing to protect from influenza, as well as the perceived likelihood of vaccine-related side effects and their severity were negatively associated with vaccine uptake. 3.5. Pertussis vaccination coverage
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26.2 (22.0–31.0) 21.1 (17.1–25.7) 19.0 (15.4–23.4) 12.9 (9.8–16.8) 11.1 (8.3–14.8) 40.3 (36.5–44.3) 30.1 (26.5–33.8) 28.5 (25.1–32.2) 18.7 (15.8–22.1) 8.6 (6.6–11.0) 8.5 (6.5–10.9) 4.9 (3.5–7.0) 0.3 (0.1–0.9)
Multiple answers were allowed. b Weighted data. c Further reasons were mentioned by unvaccinated pregnant women who did not trust the vaccine (n = 405).
While 22.5% (95% CI 20.0–25.3; crude: 24.3%) of pregnant women stated having been vaccinated against pertussis within the last 10 years, 10.5% (95% CI 8.7–12.7; crude: 10.7%) did not know their vaccination status. Having a migration background reduced the odds of being vaccinated by 48%, whereas living in the Eastern federal states and receiving seasonal influenza vaccination annually were positively associated with pertussis vaccine uptake (Table 4). When asked the hypothetical question as to whether they would comply with an official recommendation for pertussis vaccination in pregnancy, 41.5% (95% CI 37.9–45.3) of participants who were not vaccinated within the last 10 years or did not know their vaccination status stated they would be willing to receive the vaccine, 36.2% (CI 32.7–39.9%) that they would not and the remainder were unsure. 4. Discussion The aim of our study was to assess knowledge, attitudes, and behavior related to influenza vaccination among pregnant women
Please cite this article in press as: Bödeker B, et al. Cross-sectional study on factors associated with influenza vaccine uptake and pertussis vaccination status among pregnant women in Germany. Vaccine (2014), http://dx.doi.org/10.1016/j.vaccine.2014.06.007
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Fig. 2. Vaccination knowledge score of pregnant women (n = 412) in Germany by information source utilized during their pregnancy. Footnote: weighted data.
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in Germany as well as their pertussis vaccination status. Such data are crucial for the design of tailored communication strategies, but were lacking for Germany thus far. Our results revealed that – 3 years after the endorsement of the official recommendation – only 23% of women were vaccinated against influenza during pregnancy. Mistrust of influenza vaccines was the most commonly stated reason for not being vaccinated. Low to moderate influenza vaccination coverage among pregnant women has been reported also from other industrialized countries: according to a survey conducted among European Union member states, vaccination coverage among pregnant women in the 2011/12 season was around 2% in Slovenia, 30% in the United Kingdom, and 58% in Northern Ireland [12]. In the US, vaccination coverage ranged between 40% and 49% in 2010/11 and was around 47% in 2011/12 [11,16]. The differences in vaccination coverage between countries could partially be explained by different communication activities supporting the recommendation, differences in vaccination systems and funding schemes, but also different attitudes related to vaccination during pregnancy. In addition, the time evolved since the endorsement of the recommendation might influence the acceptance and eventually vaccination coverage. For example, in the US influenza vaccination was recommended for pregnant women in 1997 [32], while in Germany this recommendation was endorsed in 2010. In our study the most frequently reported reasons for women not being vaccinated against influenza were lack of confidence in the vaccine as well as poor awareness of the need for vaccination and of the existence of an official recommendation. In several other studies from industrialized countries, vaccine safety issues were a frequently mentioned concern [15–17,33,34]. In addition, some of the above-mentioned studies showed that many women were insufficiently informed about the risk of influenza during
pregnancy and the benefits of vaccination [15,33,34]. Yudin et al. showed that almost 90% of pregnant women in Toronto incorrectly thought they had the same risk of influenza-related complications as non-pregnant women, and only 40% of women knew about the recommendations for influenza vaccination in pregnancy [34]. According to studies in the US and Switzerland, 11% [16] and 16% [33] of unvaccinated women, respectively, did not believe that available vaccines are effective in preventing seasonal influenza. Of concern is that 29% of unvaccinated women in our study stated being in principle opposed to vaccinations (i.e. 19.3% of all participating women). Even though we did not specify the frame of this question in more detail, we assume that participants referred the question to vaccinations during pregnancy in general. This finding is consistent with other recently published results from Switzerland demonstrating that 23% of pregnant women held an anti-vaccine attitude during their pregnancy [33]. In Germany, little is known about vaccine skeptics and opponents. It is assumed that – independent of pregnancy – 3–5% of the German population are strictly opposed to vaccinations [35]. According to a recent study conducted among adolescents and adults in Germany, 31% had some prejudice against particular vaccines, but only 4% of them strictly opposed immunizations [36]. In our study, women stated having utilized a wide variety of sources to obtain information on influenza vaccination during pregnancy. The most frequently used sources were physicians and printed media. Especially gynecologists, who are responsible for prenatal care in Germany and therefore have regular contact with pregnant women, play an important role. Women who stated the need for more information mentioned both gynecologists and general practitioners as desired sources for further evidence. These findings are consistent with recently published studies [15,33,37]. Therefore, it seems obvious that these physician-groups should be
Please cite this article in press as: Bödeker B, et al. Cross-sectional study on factors associated with influenza vaccine uptake and pertussis vaccination status among pregnant women in Germany. Vaccine (2014), http://dx.doi.org/10.1016/j.vaccine.2014.06.007
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Table 3 Factors potentially associated with influenza vaccine uptake during pregnancy, Germany, 2012/13. Vaccination coverage, %a,b
Univariate OR (95% confidence)a,b
Multivariate OR (95% confidence)a,c
19.1
1.33 (0.87–2.04)g
NS
No Place of residence Eastern Federal States Western Federal States First pregnancy Yes No Underlying chronic disease Yes No Use of alternative medicine Often Sometimes Never Vaccination during 2011/12 season Yes No Received vaccination advice from a physician during 2012/13 season Yes No Infection with influenza during pregnancy can adversely affect pregnancy Agreed correctly Disagreed incorrectly Regular hand-washing with soap can reduce the risk of influenza infection Agreed correctly Disagreed incorrectly Generally, influenza in newborns is less severe than in older children Disagreed correctly Agreed incorrectly After immunization or infection with influenza, vaccination in ensuing influenza season is not necessary Disagreed correctly Agreed incorrectly Vaccination-knowledge-score Low Moderate Good High
15.1
Ref.
25.6 14.2
2.08 (1.38–3.13)** Ref.
NS
13.9 17.8
Ref. 1.34 (0.94–1.90)g
NS
22.1 15.4
1.56 (0.87–2.79)g Ref.
NS
9.3 14.6 18.2
Ref. 1.66 (0.81–3.42)g 2.17 (1.09–4.30)*
NS
52.4 5.7
18.11 (12.05–27.24)** Ref.
2.38 (1.33–4.24)* Ref.
40.7 1.6
43.38 (22.58–83.34)** Ref.
9.90 (4.81–20.38)** Ref.
19.7 3.8
6.18 (2.94–12.99)** Ref.
NS
15.1 20.5
0.69 (0.44–1.08)g Ref.
0.38 (0.2–0.75)* Ref.
17.4 13.9
1.3 (0.90–1.89)g Ref.
NS
17.2 13.2
1.36 (0.92–2.03)g Ref.
NS
0.6 3.4 23.3 58.0
Ref. 2.26 (0.54–9.57) 3.99 (1.08–14.70)* 5.97 (1.45–24.55)*
Perceived probability of getting infected with influenza during pregnancy when not immunizedd Perceived severity of influenza during pregnancy when not immunizede Perceived vaccine effectiveness for pregnant womenf Perceived probability of side effects for pregnant women after vaccinationd Perceived severity of side effects for pregnant women after vaccinatione
–
Ref. 5.57 (1.40–22.19)* 47.82 (14.33–159.51)** 217.61 (63.55–745.10)** 1.02 (1.01–1.03)**
–
1.69 (1.54–1.87)**
1.38 (1.21–1.59)**
– –
2.28 (1.97–2.63)** 0.93 (0.91–0.94)**
NS 0.97 (0.95–0.99)*
–
0.64 (0.58–0.70)**
0.83 (0.72–0.95)*
Migration backround Yes
NS
Other nonsignificant variables in univariate analysis (p ≥ 0.2) were: age, education level, items focusing on influenza-related knowledge. NS: not significant; Ref.: reference category. a Weighted data. b Included participants with information on relevant item. c Included n = 994 participants with complete information on all items. d Range 0–100. e Range 1–10 (“not serious” to “very serious”). f Range 1–10 (“not effective” to “very effective”). g p < 0.2 in univariate analysis. * p < 0.05. ** p < 0.001.
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a major target for information campaigns and be enabled to serve as facilitators. Our analysis suggests that influenza vaccine uptake during pregnancy is associated with a variety of different factors including level of knowledge and perceptions related to the disease and the
vaccine. Similar to studies also focusing on other vaccination targetgroups, having received an advice from a healthcare provider had the strongest influence on vaccine uptake, which once again highlights the important role of physicians in obtaining high vaccination coverage [11,16,17,25,33,37–40].
Please cite this article in press as: Bödeker B, et al. Cross-sectional study on factors associated with influenza vaccine uptake and pertussis vaccination status among pregnant women in Germany. Vaccine (2014), http://dx.doi.org/10.1016/j.vaccine.2014.06.007
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Table 4 Factors potentially associated with pertussis vaccine uptake within the last 10 years assessed among pregnant women, Germany, 2012/13.
Migration background Yes No Highest education Low Middle High Place of residence Eastern Federal States Western Federal States Underlying chronic disease Yes No Use of alternative medicine Often Sometimes Never Annual receipt of seasonal influenza vaccination Yes No
Vaccination coverage, %a,b
Univariate OR(95% confidence)a,b
Multivariate OR(95% confidence)a,c
15.3 27.8
0.47 (0.30–0.73)* Ref.
0.52 (0.33–0.83)* Ref.
17.5 25.4 30.4
Ref. 1.61 (1.03–2.51)* 2.06 (1.32–3.23)*
NS
46.6 21.4
3.21 (2.21–4.64)** Ref.
2.21 (1.47–3.34)** Ref.
34.1 24.3
1.61 (0.97–2.68)d Ref.
NS
20.0 27.4 24.8
Ref. 1.51 (0.86–2.67)d 1.32 (0.77–2.28)
NS
44.6 20.6
3.11 (2.15–4.48)** Ref.
2.60 (1.74–3.88)** Ref.
Only other nonsignificant variable in univariate analysis (p ≥ 0.2) was age. NS: not significant; Ref.: reference category. a Weighted data. b Included participants with information on relevant item. c Included n = 910 participants with complete information on all items. d p < 0.2 in univariate analysis. * p < 0.05. ** p < 0.001.
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Since there is no validated indicator for the assessment of influenza vaccine-related knowledge, the level of knowledge is measured differently from study to study. This makes the comparison of results difficult. In our study, we developed a 4-level vaccination knowledge score that showed good internal consistency and was correlated with influenza vaccine uptake in a dose–response fashion. We also found an independent negative association between influenza vaccine uptake and the belief that regular hand-washing with soap can reduce the risk of influenza infection. This finding is of high public health relevance suggesting that women believe that maintaining proper hygiene habits is sufficient to prevent influenza. Therefore it should be more clearly communicated that good hygiene practices are important, but constitute only one of several pillars for the prevention of influenza, with vaccination being the most effective intervention. In total, 23% of pregnant women had received a pertussis vaccine within the last 10 years. Two studies conducted in Germany between 2008 and 2011 revealed vaccination coverage ranging from 9% to 31% in this age-group [41,42]. In one study, a higher pertussis vaccine uptake was also noted in the eastern federal states, which might be due to experiences of the population with mandatory immunization practices until German reunification in 1990 and due to different vaccination policies at the federal state level thereafter [41]. Since migrants in Germany have been shown to utilize health services less frequently [43] and since pertussis vaccination is not recommended for pregnant women and is therefore not part of a well-organized prevention program, a negative association between a migration background and pertussis vaccine uptake within the last 10 years is plausible. This finding is supported by results from a study in the general population in Germany in 2009, that also demonstrated a lower pertussis vaccine uptake among people with migration background [41]. The proportion of women willing to obtain pertussis vaccination during pregnancy if this were recommended officially was low at 42%, but still higher than the observed influenza and pertussis vaccination coverage. This figure, however, must be interpreted with caution, since stated vaccine intentions often overestimate vaccination coverage eventually achieved [44,45]. A willingness of 42% still reflects a high
degree of skepticism and uncertainty regarding vaccination during pregnancy that must be adequately addressed. In other studies the most frequently mentioned reasons for refusal of pertussis vaccination in pregnancy were safety concerns [46,47]. In Germany, the current strategy for the prevention of pertussis in infants is the cocooning strategy. However, as reflected by low pertussis vaccination coverage among pregnant women shown in our study and a coverage of only 10% among persons with close contact to infants shown previously [41], this strategy has not led to high uptake, likely because it is not embedded in a concerted program. Implementation of a pregnancy-based vaccination strategy may be more feasible. Therefore, in addition to data on pertussis vaccine safety in pregnancy and protective effects on infants, indicators predicting the likely acceptance of pertussis vaccination in pregnancy would be helpful to guide future policy decisions. One potential limitation of our study is that the vaccination status was self-reported and can therefore be subject to recall bias. While previous studies demonstrated an adequate degree of reliability for self-reported influenza vaccination status in adults [48,49], the validity of self-reported pertussis vaccination status seemed to be rather poor, often overestimating vaccination coverage [50,51]. Furthermore, due to our recruitment strategy it was not possible to calculate the response rate, since the total number of women asked to participate is unknown. In other studies targeting the behavior and attitudes of pregnant women, response rates were usually very high, which can be explained by an increased interest in health-related topics during pregnancy [47,52]. Thus, while this is likely the case in our study as well, we cannot fully rule out that some degree of selection bias was present. Another limitation was the exclusion of women with insufficient knowledge of the German language, which might affect the vaccination coverage assessed for women with migration background and its relevance as a factor influencing vaccine uptake. However, several other important characteristics such as migration background and the proportion of foreign born individuals were similar to that of the general female population, which is a result of the recruitment strategy, the large study sample, and the weighting procedures. Since no representative national perinatal dataset exists, we
Please cite this article in press as: Bödeker B, et al. Cross-sectional study on factors associated with influenza vaccine uptake and pertussis vaccination status among pregnant women in Germany. Vaccine (2014), http://dx.doi.org/10.1016/j.vaccine.2014.06.007
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compared characteristics of our study sample with that of women of childbearing age living in Germany. In conclusion, STIKO-recommendations related to the protection of pregnant woman and newborns against seasonal influenza and pertussis are not effectively implemented in Germany. Special efforts must be undertaken to enhance influenza vaccine uptake. In this context, especially gynecologists play an important role and should be included as a major target group in communication activities. Both pregnant women and gynecologists need to be adequately informed about risks and benefits of influenza vaccines as well as disease-related risks. Education of physicians and women is also needed to increase the awareness of the current STIKOrecommendations for pertussis vaccination and to underline the importance of being immunized before pregnancy or shortly after delivery to indirectly protect the infant. While pertussis vaccination is currently not part of the antenatal care program in Germany, gynecologists should nonetheless offer pregnant women postnatal pertussis vaccination if not already vaccinated and inform them of the need for timely vaccination of other members of the household to protect infants from pertussis. Monitoring tools should be implemented to investigate vaccination coverage among pregnant women as well as the effectiveness of both interventions. Contributions All authors were involved in the conception and design of the study. BB performed the data analysis and drafted the article. All authors contributed to the data interpretation and finalization of the manuscript. Conflict of interest The authors have declared no conflicts of interest. Acknowledgments
We would like to thank all pregnant women who participated in the study and Wiebke Hellenbrand (RKI) who provide important 447 Q2 input in the discussions around pertussis. The study was funded by 448 Q3 the Federal Ministry of Health. 449 446
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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;176:463–8. [2] Schanzer DL, Langley JM, Tam TW. Influenza-attributed hospitalization rates among pregnant women in Canada 1994-2000. J Obstet Gynaecol Can 2007;29:622–9. [3] Rasmussen SA, Jamieson DJ, Uyeki TM. Effects of influenza on pregnant women and infants. Am J Obstet Gynecol 2012;207:S3–8. [4] Omer SB, Goodman D, Steinhoff MC, Rochat R, Klugman KP, Stoll BJ, et al. Maternal influenza immunization and reduced likelihood of prematurity and small for gestational age births: a retrospective cohort study. PLoS Med 2011;8:e1000441. [5] Hardy JM, Azarowicz EN, Mannini A, Medearis Jr DN, Cooke RE. The effect of Asian influenza on the outcome of pregnancy Baltimore, 1957-1958. Am J Public Health Nation’s Health 1961;51:1182–8. [6] Eick AA, Uyeki TM, Klimov A, Hall H, Reid R, Santosham M, et al. Maternal influenza vaccination and effect on influenza virus infection in young infants. Arch Pediatr Adolesc Med 2011;165:104–11. [7] Sheffield JS, Greer LG, Rogers VL, Roberts SW, Lytle H, McIntire DD, et al. Effect of influenza vaccination in the first trimester of pregnancy. Obstet Gynecol 2012;120:532–7. [8] 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. [9] Poehling KA, Szilagyi PG, Staat MA, Snively BM, Payne DC, Bridges CB, et al. Impact of maternal immunization on influenza hospitalizations in infants. Am J Obstet Gynecol 2011;204:S141–8.
[10] World Health Organization. Meeting of the strategic advisory group of experts on immunization April 2012 – conclusions and recommendations. Wkly Epidemiol Rec 2012;21:201–16. [11] Kennedy ED, Ahluwalia IB, Ding H, Lu PJ, Singleton JA, Bridges CB. Monitoring seasonal influenza vaccination coverage among pregnant women in the United States. Am J Obstet Gynecol 2012;207:S9–16. [12] O’Flanagan D, Cotter S, Mereckiene J. Seasonal influenza vaccination in EU/EEA, influenza season 2011-12 [cited November 15th 2013]; 2013 http://venice.cineca.org/VENICE Seasonal Influenza 2011-12 1.0v.pdf [13] Robert Koch Institute. Mitteilung der Ständigen Impfkommission (STIKO) am Robert Koch-Institut: Änderung der Empfehlung zur Impfung gegen Influenza. Epid Bull 2010;31:299–309. [14] Vetter K, Goeckenjan M. [Prenatal care in Germany]. Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz 2013;56:1679–85. [15] Eppes C, Wu A, You W, Cameron KA, Garcia P, Grobman W. Barriers to influenza vaccination among pregnant women. Vaccine 2013;31:2874–8. [16] Centers for Disease Control Prevention. Influenza vaccination coverage among pregnant women – 2011-12 influenza season, United States. MMWR Morb Mortal Wkly Rep 2012;61:758–63. [17] Wiley KE, Massey PD, Cooper SC, Wood NJ, Ho J, Quinn HE, et al. Uptake of influenza vaccine by pregnant women: a cross-sectional survey. Med J Aust 2013;198:373–5. [18] Blanchard-Rohner G, Siegrist CA. Vaccination during pregnancy to protect infants against influenza: why and why not? Vaccine 2011;29:7542–50. [19] Gall SA. Prevention of pertussis, tetanus, and diphtheria among pregnant, postpartum women, and infants. Clin Obstet Gynecol 2012;55:498–509. [20] Greenberg DP, von Koenig CH, Heininger U. Health burden of pertussis in infants and children. Pediatr Infect Dis J 2005;24:S39–43. [21] Robert Koch Institute. Empfehlungen der Ständigen Impfkommission (STIKO) am Robert Koch-Institut/Stand: Juli 2004. Epid Bull 2004;30:235–50. [22] Centers for Disease Control Prevention. Updated recommendations for use of tetanus toxoid reduced diphtheria toxoid and acellular pertussis vaccine (Tdap) in pregnant women and persons who have or anticipate having close contact with an infant aged
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Contents lists available at ScienceDirect
Vaccine journal homepage: www.elsevier.com/locate/vaccine
Cross-sectional study on factors associated with influenza vaccine uptake and pertussis vaccination status among pregnant women in Germany
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Birte Bödeker a,b,∗ , Dietmar Walter a , Sabine Reiter a , Ole Wichmann a a b
Immunization Unit, Robert Koch Institute, Seestraße 10, 13353 Berlin, Germany Charité – University Medicine Berlin, Augustenburger Platz 1, 13353 Berlin, Germany
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Article history: Received 5 December 2013 Received in revised form 7 May 2014 Accepted 2 June 2014 Available online xxx
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Keywords: Pregnancy Influenza Pertussis Vaccination Attitude Knowledge
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1. Introduction
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Pregnant women and their newborns are at increased risk for influenza-related complications; the latter also have an increased risk for pertussis-related complications. In Germany, seasonal influenza vaccination is recommended for pregnant women since 2010. A dose of pertussis-containing vaccine has been recommended since 2004 for women of childbearing age if they have not been vaccinated within the past 10 years. We conducted a nationwide cross-sectional survey among pregnant women in February/March 2013 to assess knowledge, attitudes, and practices related to influenza vaccination during pregnancy and to identify factors associated with their pertussis vaccination status. In total, 1025 pregnant women participated and provided information through a self-administered questionnaire. Of these, 23.2% were vaccinated against seasonal influenza during the 2012/13 season; 15.9% during their pregnancy. Major reasons for being unvaccinated (n = 686 respondents) were lack of confidence in the vaccine (60.4%) and the perception that vaccination was not necessary (40.3%). Influenza vaccination during pregnancy was independently associated with having received influenza vaccine in the previous season, having received a recommendation from a physician, a high level of vaccine-related knowledge and of perceived disease severity. In contrast, knowledge of the recommendation for regular hand-washing to prevent influenza and the perception that vaccine-related side effects were likely to occur or likely to be severe were negatively associated with vaccine uptake. Receipt of a pertussis vaccine in the past 10 years was reported by 22.5% of participants. Pertussis vaccine uptake was independently associated with living in the Eastern federal states and receiving seasonal influenza vaccination annually, while a migration background was associated with a lower uptake. To enhance vaccine uptake in pregnant women and women of childbearing age, special efforts must be undertaken to improve knowledge of both recommendations and the benefits of vaccination. Gynecologists could serve as important facilitators. © 2014 Published by Elsevier Ltd.
Both pregnant women and newborns are at increased risk for influenza-related complications and hospitalization [1–3]. Influenza during pregnancy can cause stillbirth, preterm delivery, and growth retardation in the child [4,5]. Studies have demonstrated that influenza vaccination during pregnancy is safe and can effectively prevent influenza illness in pregnant women and also their newborns [6–9]. For these reasons, the World Health
∗ Corresponding author at: Immunization Unit, Robert Koch Institute, Seestrasse 10, 13353 Berlin, Germany. Tel.: +49 30 18754 3215; fax: +49 30 18754 3533. E-mail address: [email protected] (B. Bödeker).
Organization declared pregnant women as a group to be targeted by seasonal influenza vaccination with highest priority [10]. Despite compelling evidence on the safety and benefits of influenza vaccination during pregnancy, data from industrialized countries suggest only a low to moderate vaccine uptake in this target-group [11,12]. In Germany, seasonal influenza vaccination was recommended in August 2010 for all pregnant women from the 2nd trimester and for pregnant women with underlying chronic disease from the 1st trimester [13]. However, in the absence of an immunization registry no data on the vaccine uptake in this target-group is available thus far. In Germany, antenatal care is based on a nationwide standardized program for all pregnant women that is fully funded by health insurances and provided by office-based gynecologists, midwives and maternity clinics. Primary prenatal care including
http://dx.doi.org/10.1016/j.vaccine.2014.06.007 0264-410X/© 2014 Published by Elsevier Ltd.
Please cite this article in press as: Bödeker B, et al. Cross-sectional study on factors associated with influenza vaccine uptake and pertussis vaccination status among pregnant women in Germany. Vaccine (2014), http://dx.doi.org/10.1016/j.vaccine.2014.06.007
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pregnancy-related vaccination is primarily provided by officebased gynecologists [14]. Knowledge on the perceptions of pregnant women regarding influenza and on barriers and promoters for their decision to receive influenza vaccine are crucial to design tailored communication strategies and to increase vaccination coverage. Some studies reported on barriers such as vaccine safety concerns, mistrust in the vaccine, low risk perception of the disease, and poor vaccinerelated knowledge [15–18]. However, several of these studies had limitations due to their study design and small sample size, and knowledge/attitude among pregnant women may considerably vary from country to country. Similar to influenza, pertussis infection is associated with an increased risk for complications in infants when compared to other age-groups [19,20]. Since 2004, the German Standing Committee on Vaccination (STIKO) recommends pertussis vaccination for women of childbearing age as well for all close contacts of infants who have not received a pertussis vaccination within the past 10 years (so-called cocooning strategy). If a pregnant woman is not vaccinated before conception, STIKO recommends vaccination preferably in the first days after the birth of the child [21]. In contrast to the US or the United Kingdom, pertussis vaccination of pregnant women is currently not recommended in Germany [22,23]. We conducted a nationwide cross-sectional study among pregnant women aged 18 years and older living in Germany to assess influenza vaccine uptake during the 2012/13 season and pertussis vaccine uptake in the previous 10 years. In particular we aimed to assess knowledge of and attitudes towards seasonal influenza vaccination in this target-group.
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We conducted a nationwide cross-sectional survey among pregnant women between February and March 2013. The interviews were conducted by USUMA GmbH, a professional market and research company. Pregnant women were recruited based on a special sampling frame designed as an area sample (ADMSampling-System for Face-to-Face Surveys), which allows the assembly of representative samples for Germany [24]. Inclusion criteria for study participation were (i) being at least 18 years of age, (ii) being at least 12 weeks pregnant, and (iii) having a good command of the German language as assessed by study assistants responsible for the recruitment and data collection process in an area. Women were recruited in different ways: either (i) direct outreach, whereby pregnant women were invited to participate by our study assistants at specific sampling points in places where pregnant women typically congregate (e.g. gynecologist’s office, midwife’s office, maternity clinic), (ii) distribution of information leaflets by study assistants in these places inviting women to contact them by phone if interested in participating, or (iii) asking women to inform other pregnant women about the study. To obtain a study sample approximately representative for factors relevant to the study question, recruitment procedures included the use of quota proportions for specific population characteristics (age, educational status, and nationality) that were previously associated with vaccination against seasonal or pandemic influenza in the general population in Germany [25–27]. For this purpose, at the beginning of the survey study assistants were provided with quotas derived from different datasets gathered by the Federal Statistical Office of Germany to be met during recruitment. Since no representative perinatal dataset was available for Germany, quotas were based on data of mothers’ average age at the time of giving
birth, on educational level of women of childbearing age, and on nationality of newborns and their parents, respectively. All interested pregnant women were informed about the background, the objectives and the data protection and privacy related to this study. After providing verbal consent, participating women completed an anonymous, self-administered questionnaire that they returned directly to the study assistant. Participants did not receive any incentives. The institutional data protection officer of the Robert Koch Institute approved the study protocol; since no personal or clinical data were collected during the survey, an approval by the German Federal Commissioner for Data Protection and Freedom of Information was not required. 2.2. Study questionnaire and definitions The questionnaire elicited socio-economic and demographic data as well as information on knowledge, attitudes, and behavior regarding seasonal influenza vaccination and the disease, information needs concerning influenza vaccination, pertussis vaccination status, as well as women’s health status. Some of the sociodemographic items were used in previous surveys (such as the GEDA [28]), but were adapted to our setting. Further survey items were developed by reviewing the international literature. We applied single-item scales to the majority of items. Before study implementation, the questionnaire was pretested and subsequently modified. To assess the influenza vaccination status for season 2012/13, we asked whether the women had been vaccinated since 1st September 2012 and whether this was during or before their pregnancy. Furthermore, we asked for any pertussis vaccination within the last 10 years. We assessed disease- and vaccination-related knowledge of influenza. For this purpose, participants were asked to give their level of agreement with different statements that were answered on a 4-point Likert scale supplemented with the option of “don’t know”. Under the assumption that both incorrect as well as lack of knowledge reflect a lack of awareness for the importance of obtaining vaccination, we collapsed responses into two categories “agreed/disagreed correctly” vs. “agreed/disagreed incorrectly”, in which “don’t know” was assigned to “incorrect”. Vaccination-related questions were summed to obtain a knowledge score (range 0–4). We tested the scale’s internal consistency and excluded one item to obtain a final Cronbachs ∝ of 0.7. Based on the distribution of quartiles, the range of vaccination knowledge score was divided into four levels of knowledge. Migration background was defined as described by Schenk et al. on the basis of parents’ country of birth [29]. 2.3. Data analysis To control for possible selection biases, weighting factors were constructed. Since results of previous studies demonstrated that in Germany both age and place of residence were associated with influenza vaccine uptake in the general population [25,30], and since the above-mentioned quotas were not always fully met and did not take into account region-specific differences, we used the number of live births per federal state and per mother’s year of birth to calculate respective weighting factors. These factors were created on the basis of population data gathered by the Federal Statistical Office of Germany for 2011 [31]. Statistical analysis was performed using StataSE12 (StataCorp LP, College Station, Texas, US) using complex survey methods. Univariate and multivariate logistic regression analysis was applied to determine a potential association between influenza vaccine uptake during pregnancy and demographic characteristics, health-relevant factors, as well as attitude and knowledge. Odds ratios (OR) and 95% confidence intervals (CI) were calculated. Statistical significance was accorded when p < 0.05. All variables
Please cite this article in press as: Bödeker B, et al. Cross-sectional study on factors associated with influenza vaccine uptake and pertussis vaccination status among pregnant women in Germany. Vaccine (2014), http://dx.doi.org/10.1016/j.vaccine.2014.06.007
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identified in univariate analysis to be potentially associated with influenza vaccination (p-value 0.1 from the model. We then performed adjusted Wald test for independent variables with 0.05 ≤ p ≤ 0.1 to review whether these parameters create a statistically significant improvement in the fit of the model. Due to multicollinearity we removed two variables (perceived probability and severity of side effects for the unborn child after vaccination) which supplied redundant information. We proceeded analogously to assess potential associations of pertussis vaccination in the last 10 years with demographic and health behavior factors.
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In total, 1030 pregnant women completed the survey questionnaire. Due to missing compliance with inclusion criteria five datasets were eliminated, resulting in 1025 datasets included in the final analysis. An overview of the characteristics of the study population in comparison to the general female population aged 18–49 years is provided in Table 1. The median age of women was 31 years (range 18–46) and 20.4% had a migration background. Approximately 60% of women were in the 2nd trimester of pregnancy and half were pregnant with their first child. 3.2. Influenza vaccination coverage and reasons for not being immunized During the 2012/13 season, 23.2% (95% CI: 20.6–26.0; crude without weighting: 23.4%) of pregnant women were vaccinated against seasonal influenza, whereas 15.9% (95% CI: 13.7–18.4; crude: 16.1%) received the flu shot while being pregnant. Reasons provided by the women for not being vaccinated are shown in Table 2. Among those not vaccinated and not intending to get vaccinated, more than half (60.4%) stated mistrusting the vaccine and 40.3% thought that vaccination was not necessary for them. Among those who mistrusted the vaccine, nearly two thirds (64.4%) reported fear of side effects. 3.3. Information seeking behavior regarding influenza vaccination Of all participating women, 40.5% actively sought information on influenza vaccination during pregnancy. Of these, most stated their physicians as an important information source (76.6%), followed by print media (59.7%), internet (47.6%) and relatives or friends (45%) (Fig. 1). Fig. 2 depicts the vaccination knowledge score of participants according to whether they utilized a specific information source or not. Results suggest that women who used the internet or television/radio had on average a slightly lower vaccination knowledge score compared to women seeking advice from other sources. In contrast, participants who sought advice from physicians or used print media had a significantly higher knowledge score than those who did not mention these sources. Participants who sought advice from physicians were also more often vaccinated than those who did not (39.6% vs. 7.8%, p < 0.001). There was no such association with any of the other utilized information sources. Of all participating women, 35.2% (95% CI: 32.2–38.4) reported a need for further information. Participants were particularly interested in receiving further information on vaccine-related side effects for pregnant women (78.2%) and their unborn child (73.2%) as well as on benefits for both the unborn child (76.2%) and
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Table 1 Characteristics of the study population and the general female population aged 18–49 years living in Germany in 2011. Study population, % (95% confidence)a Age-group (n = 1023) 18–24 years 25–29 years 30–34 years 35–39 years 40–49 years Country of birth (n = 1025) Germany Other country Migration background (n = 1025) Yes No Place of residence (n = 1025) Eastern Federal Statesc Western Federal States Highest educationd (n = 1025) Low Middle High Cannot be assigned Employment (n = 1021) Not employed Part-time employed Full-time employed Irregular employed Temporary suspended Monthly household income (n = 1008) ≤1500 D 1501–2000 D 2001–2500 D 2501–3000 D ≥3001 D Don’t know Family status (n = 1022) Married Civil union Single Other First pregnancy (n = 1020) Yes No Pregnancy trimester (n = 1025) Second Third
Genereral female population, % (n = 17,165,000)b
14.1 (12.3–16.1) 27.4 (24.8–30.2) 34.3 (31.2–37.6) 18.8 (16.3–21.7) 5.3 (3.8–7.3)
19.0 14.2 14.1 14.1 38.6
84.6 (82.1–86.8) 15.4 (13.2–17.9)
81.8 18.2
20.4 (17.9–23.2) 79.6 (76.8–82.1)
22.3 77.7
15.2 (13.1–17.4) 84.8 (82.6–86.9)
14.5 85.5
23.4 (20.8–26.3) 38.5 (35.4–41.7) 36.9 (33.8–40.2) 1.1 (0.6–2.0)
25.7 37.0 37.0 0.3
19.5 (17.1–22.2) 23.5 (20.7–26.4) 44.6 (41.4–47.8) 5.9 (4.5–7.6) 6.6 (5.1–8.5)
26.0 74.0e
13.3 (11.3–15.5) 13.1 (11.1–15.4) 20.8 (18.3–23.6) 23.7 (21.0–26.7) 23.4 (20.7–26.5) 5.7 (4.3–7.5)
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65.0 (61.9–68.0) 5.4 (4.1–7.0) 26.0 (23.3–28.8) 3.7 (2.6–5.1)
48.0 0.1 43.6 8.4
49.6 (46.3–52.8) 50.5 (47.2–53.7)
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62.0 (58.8–65.2) 38.0 (34.9–41.2)
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Weighted data (totals are not weighted). Data from the Federal Statistical Office of Germany [53]. c Brandenburg, Mecklenburg-Vorpommern, Saxony, Saxony-Anhalt, Thuringia. d Low: 9 years or less of school education, middle: at least 10 years of school education, high: university entrance diploma. e Includes all employed women including full-time, part-time or irregular employment as well as women who were temporary suspended b
the expectant mother (66.2%). Additional information regarding influenza-related complications during pregnancy was desired by 70.8%. Women who wished to obtain more information preferred to receive these from their gynecologists (89.2%), followed by general practitioners (50.4%) and print media (42.7%). Only one quarter of women (26.7%) mentioned the internet as desirable information source. 3.4. Factors associated with influenza vaccine uptake Results from univariate and multivariate logistic regression analysis on factors potentially associated with influenza vaccine
Please cite this article in press as: Bödeker B, et al. Cross-sectional study on factors associated with influenza vaccine uptake and pertussis vaccination status among pregnant women in Germany. Vaccine (2014), http://dx.doi.org/10.1016/j.vaccine.2014.06.007
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Proportion [%] Fig. 1. Information sources utilized by pregnant women (n = 413) in Germany to obtain information about influenza vaccination during pregnancy. Footnote: weighted data; multiple answers were allowed.
Table 2 Reasons against seasonal influenza vaccination stated by 686 unvaccinated pregnant women, Germany, 2012/13. Reasons against influenza vaccinationa
Study population, % (95% confidence)b
I dont’t trust the vaccine. . . . . . becausec . . . Fear of side-effects Family members or friends had bad experiences with influenza vaccination. . . Media discussions around vaccine safety concerned me Vaccine is not effective Vaccine isn’t tested sufficiently Other In past, I had bad experiences with influenza vaccination Vaccination is not necessary for me I don’t know that pregnant women should be vaccinated In general, I am opposed to vaccination Somebody advised me not to get vaccinated Vaccine was not offered by my physician Fear of needles Due to organisational issues/vaccination was too time-consuming Vaccine was not available at the doctor’s office
60.4 (56.5–64.3)
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64.4 (59.3–69.2) 32.9 (28.2–37.9)
uptake are shown in Table 3. Influenza vaccine uptake in 2012/13 was independently associated with influenza vaccination in the previous season, with a vaccination recommendation from a physician, a high vaccination knowledge score, and the degree of perceived disease severity. In addition, knowledge of the recommendation for regular hand-washing to protect from influenza, as well as the perceived likelihood of vaccine-related side effects and their severity were negatively associated with vaccine uptake. 3.5. Pertussis vaccination coverage
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26.2 (22.0–31.0) 21.1 (17.1–25.7) 19.0 (15.4–23.4) 12.9 (9.8–16.8) 11.1 (8.3–14.8) 40.3 (36.5–44.3) 30.1 (26.5–33.8) 28.5 (25.1–32.2) 18.7 (15.8–22.1) 8.6 (6.6–11.0) 8.5 (6.5–10.9) 4.9 (3.5–7.0) 0.3 (0.1–0.9)
Multiple answers were allowed. b Weighted data. c Further reasons were mentioned by unvaccinated pregnant women who did not trust the vaccine (n = 405).
While 22.5% (95% CI 20.0–25.3; crude: 24.3%) of pregnant women stated having been vaccinated against pertussis within the last 10 years, 10.5% (95% CI 8.7–12.7; crude: 10.7%) did not know their vaccination status. Having a migration background reduced the odds of being vaccinated by 48%, whereas living in the Eastern federal states and receiving seasonal influenza vaccination annually were positively associated with pertussis vaccine uptake (Table 4). When asked the hypothetical question as to whether they would comply with an official recommendation for pertussis vaccination in pregnancy, 41.5% (95% CI 37.9–45.3) of participants who were not vaccinated within the last 10 years or did not know their vaccination status stated they would be willing to receive the vaccine, 36.2% (CI 32.7–39.9%) that they would not and the remainder were unsure. 4. Discussion The aim of our study was to assess knowledge, attitudes, and behavior related to influenza vaccination among pregnant women
Please cite this article in press as: Bödeker B, et al. Cross-sectional study on factors associated with influenza vaccine uptake and pertussis vaccination status among pregnant women in Germany. Vaccine (2014), http://dx.doi.org/10.1016/j.vaccine.2014.06.007
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Fig. 2. Vaccination knowledge score of pregnant women (n = 412) in Germany by information source utilized during their pregnancy. Footnote: weighted data.
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in Germany as well as their pertussis vaccination status. Such data are crucial for the design of tailored communication strategies, but were lacking for Germany thus far. Our results revealed that – 3 years after the endorsement of the official recommendation – only 23% of women were vaccinated against influenza during pregnancy. Mistrust of influenza vaccines was the most commonly stated reason for not being vaccinated. Low to moderate influenza vaccination coverage among pregnant women has been reported also from other industrialized countries: according to a survey conducted among European Union member states, vaccination coverage among pregnant women in the 2011/12 season was around 2% in Slovenia, 30% in the United Kingdom, and 58% in Northern Ireland [12]. In the US, vaccination coverage ranged between 40% and 49% in 2010/11 and was around 47% in 2011/12 [11,16]. The differences in vaccination coverage between countries could partially be explained by different communication activities supporting the recommendation, differences in vaccination systems and funding schemes, but also different attitudes related to vaccination during pregnancy. In addition, the time evolved since the endorsement of the recommendation might influence the acceptance and eventually vaccination coverage. For example, in the US influenza vaccination was recommended for pregnant women in 1997 [32], while in Germany this recommendation was endorsed in 2010. In our study the most frequently reported reasons for women not being vaccinated against influenza were lack of confidence in the vaccine as well as poor awareness of the need for vaccination and of the existence of an official recommendation. In several other studies from industrialized countries, vaccine safety issues were a frequently mentioned concern [15–17,33,34]. In addition, some of the above-mentioned studies showed that many women were insufficiently informed about the risk of influenza during
pregnancy and the benefits of vaccination [15,33,34]. Yudin et al. showed that almost 90% of pregnant women in Toronto incorrectly thought they had the same risk of influenza-related complications as non-pregnant women, and only 40% of women knew about the recommendations for influenza vaccination in pregnancy [34]. According to studies in the US and Switzerland, 11% [16] and 16% [33] of unvaccinated women, respectively, did not believe that available vaccines are effective in preventing seasonal influenza. Of concern is that 29% of unvaccinated women in our study stated being in principle opposed to vaccinations (i.e. 19.3% of all participating women). Even though we did not specify the frame of this question in more detail, we assume that participants referred the question to vaccinations during pregnancy in general. This finding is consistent with other recently published results from Switzerland demonstrating that 23% of pregnant women held an anti-vaccine attitude during their pregnancy [33]. In Germany, little is known about vaccine skeptics and opponents. It is assumed that – independent of pregnancy – 3–5% of the German population are strictly opposed to vaccinations [35]. According to a recent study conducted among adolescents and adults in Germany, 31% had some prejudice against particular vaccines, but only 4% of them strictly opposed immunizations [36]. In our study, women stated having utilized a wide variety of sources to obtain information on influenza vaccination during pregnancy. The most frequently used sources were physicians and printed media. Especially gynecologists, who are responsible for prenatal care in Germany and therefore have regular contact with pregnant women, play an important role. Women who stated the need for more information mentioned both gynecologists and general practitioners as desired sources for further evidence. These findings are consistent with recently published studies [15,33,37]. Therefore, it seems obvious that these physician-groups should be
Please cite this article in press as: Bödeker B, et al. Cross-sectional study on factors associated with influenza vaccine uptake and pertussis vaccination status among pregnant women in Germany. Vaccine (2014), http://dx.doi.org/10.1016/j.vaccine.2014.06.007
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Table 3 Factors potentially associated with influenza vaccine uptake during pregnancy, Germany, 2012/13. Vaccination coverage, %a,b
Univariate OR (95% confidence)a,b
Multivariate OR (95% confidence)a,c
19.1
1.33 (0.87–2.04)g
NS
No Place of residence Eastern Federal States Western Federal States First pregnancy Yes No Underlying chronic disease Yes No Use of alternative medicine Often Sometimes Never Vaccination during 2011/12 season Yes No Received vaccination advice from a physician during 2012/13 season Yes No Infection with influenza during pregnancy can adversely affect pregnancy Agreed correctly Disagreed incorrectly Regular hand-washing with soap can reduce the risk of influenza infection Agreed correctly Disagreed incorrectly Generally, influenza in newborns is less severe than in older children Disagreed correctly Agreed incorrectly After immunization or infection with influenza, vaccination in ensuing influenza season is not necessary Disagreed correctly Agreed incorrectly Vaccination-knowledge-score Low Moderate Good High
15.1
Ref.
25.6 14.2
2.08 (1.38–3.13)** Ref.
NS
13.9 17.8
Ref. 1.34 (0.94–1.90)g
NS
22.1 15.4
1.56 (0.87–2.79)g Ref.
NS
9.3 14.6 18.2
Ref. 1.66 (0.81–3.42)g 2.17 (1.09–4.30)*
NS
52.4 5.7
18.11 (12.05–27.24)** Ref.
2.38 (1.33–4.24)* Ref.
40.7 1.6
43.38 (22.58–83.34)** Ref.
9.90 (4.81–20.38)** Ref.
19.7 3.8
6.18 (2.94–12.99)** Ref.
NS
15.1 20.5
0.69 (0.44–1.08)g Ref.
0.38 (0.2–0.75)* Ref.
17.4 13.9
1.3 (0.90–1.89)g Ref.
NS
17.2 13.2
1.36 (0.92–2.03)g Ref.
NS
0.6 3.4 23.3 58.0
Ref. 2.26 (0.54–9.57) 3.99 (1.08–14.70)* 5.97 (1.45–24.55)*
Perceived probability of getting infected with influenza during pregnancy when not immunizedd Perceived severity of influenza during pregnancy when not immunizede Perceived vaccine effectiveness for pregnant womenf Perceived probability of side effects for pregnant women after vaccinationd Perceived severity of side effects for pregnant women after vaccinatione
–
Ref. 5.57 (1.40–22.19)* 47.82 (14.33–159.51)** 217.61 (63.55–745.10)** 1.02 (1.01–1.03)**
–
1.69 (1.54–1.87)**
1.38 (1.21–1.59)**
– –
2.28 (1.97–2.63)** 0.93 (0.91–0.94)**
NS 0.97 (0.95–0.99)*
–
0.64 (0.58–0.70)**
0.83 (0.72–0.95)*
Migration backround Yes
NS
Other nonsignificant variables in univariate analysis (p ≥ 0.2) were: age, education level, items focusing on influenza-related knowledge. NS: not significant; Ref.: reference category. a Weighted data. b Included participants with information on relevant item. c Included n = 994 participants with complete information on all items. d Range 0–100. e Range 1–10 (“not serious” to “very serious”). f Range 1–10 (“not effective” to “very effective”). g p < 0.2 in univariate analysis. * p < 0.05. ** p < 0.001.
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a major target for information campaigns and be enabled to serve as facilitators. Our analysis suggests that influenza vaccine uptake during pregnancy is associated with a variety of different factors including level of knowledge and perceptions related to the disease and the
vaccine. Similar to studies also focusing on other vaccination targetgroups, having received an advice from a healthcare provider had the strongest influence on vaccine uptake, which once again highlights the important role of physicians in obtaining high vaccination coverage [11,16,17,25,33,37–40].
Please cite this article in press as: Bödeker B, et al. Cross-sectional study on factors associated with influenza vaccine uptake and pertussis vaccination status among pregnant women in Germany. Vaccine (2014), http://dx.doi.org/10.1016/j.vaccine.2014.06.007
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Table 4 Factors potentially associated with pertussis vaccine uptake within the last 10 years assessed among pregnant women, Germany, 2012/13.
Migration background Yes No Highest education Low Middle High Place of residence Eastern Federal States Western Federal States Underlying chronic disease Yes No Use of alternative medicine Often Sometimes Never Annual receipt of seasonal influenza vaccination Yes No
Vaccination coverage, %a,b
Univariate OR(95% confidence)a,b
Multivariate OR(95% confidence)a,c
15.3 27.8
0.47 (0.30–0.73)* Ref.
0.52 (0.33–0.83)* Ref.
17.5 25.4 30.4
Ref. 1.61 (1.03–2.51)* 2.06 (1.32–3.23)*
NS
46.6 21.4
3.21 (2.21–4.64)** Ref.
2.21 (1.47–3.34)** Ref.
34.1 24.3
1.61 (0.97–2.68)d Ref.
NS
20.0 27.4 24.8
Ref. 1.51 (0.86–2.67)d 1.32 (0.77–2.28)
NS
44.6 20.6
3.11 (2.15–4.48)** Ref.
2.60 (1.74–3.88)** Ref.
Only other nonsignificant variable in univariate analysis (p ≥ 0.2) was age. NS: not significant; Ref.: reference category. a Weighted data. b Included participants with information on relevant item. c Included n = 910 participants with complete information on all items. d p < 0.2 in univariate analysis. * p < 0.05. ** p < 0.001.
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Since there is no validated indicator for the assessment of influenza vaccine-related knowledge, the level of knowledge is measured differently from study to study. This makes the comparison of results difficult. In our study, we developed a 4-level vaccination knowledge score that showed good internal consistency and was correlated with influenza vaccine uptake in a dose–response fashion. We also found an independent negative association between influenza vaccine uptake and the belief that regular hand-washing with soap can reduce the risk of influenza infection. This finding is of high public health relevance suggesting that women believe that maintaining proper hygiene habits is sufficient to prevent influenza. Therefore it should be more clearly communicated that good hygiene practices are important, but constitute only one of several pillars for the prevention of influenza, with vaccination being the most effective intervention. In total, 23% of pregnant women had received a pertussis vaccine within the last 10 years. Two studies conducted in Germany between 2008 and 2011 revealed vaccination coverage ranging from 9% to 31% in this age-group [41,42]. In one study, a higher pertussis vaccine uptake was also noted in the eastern federal states, which might be due to experiences of the population with mandatory immunization practices until German reunification in 1990 and due to different vaccination policies at the federal state level thereafter [41]. Since migrants in Germany have been shown to utilize health services less frequently [43] and since pertussis vaccination is not recommended for pregnant women and is therefore not part of a well-organized prevention program, a negative association between a migration background and pertussis vaccine uptake within the last 10 years is plausible. This finding is supported by results from a study in the general population in Germany in 2009, that also demonstrated a lower pertussis vaccine uptake among people with migration background [41]. The proportion of women willing to obtain pertussis vaccination during pregnancy if this were recommended officially was low at 42%, but still higher than the observed influenza and pertussis vaccination coverage. This figure, however, must be interpreted with caution, since stated vaccine intentions often overestimate vaccination coverage eventually achieved [44,45]. A willingness of 42% still reflects a high
degree of skepticism and uncertainty regarding vaccination during pregnancy that must be adequately addressed. In other studies the most frequently mentioned reasons for refusal of pertussis vaccination in pregnancy were safety concerns [46,47]. In Germany, the current strategy for the prevention of pertussis in infants is the cocooning strategy. However, as reflected by low pertussis vaccination coverage among pregnant women shown in our study and a coverage of only 10% among persons with close contact to infants shown previously [41], this strategy has not led to high uptake, likely because it is not embedded in a concerted program. Implementation of a pregnancy-based vaccination strategy may be more feasible. Therefore, in addition to data on pertussis vaccine safety in pregnancy and protective effects on infants, indicators predicting the likely acceptance of pertussis vaccination in pregnancy would be helpful to guide future policy decisions. One potential limitation of our study is that the vaccination status was self-reported and can therefore be subject to recall bias. While previous studies demonstrated an adequate degree of reliability for self-reported influenza vaccination status in adults [48,49], the validity of self-reported pertussis vaccination status seemed to be rather poor, often overestimating vaccination coverage [50,51]. Furthermore, due to our recruitment strategy it was not possible to calculate the response rate, since the total number of women asked to participate is unknown. In other studies targeting the behavior and attitudes of pregnant women, response rates were usually very high, which can be explained by an increased interest in health-related topics during pregnancy [47,52]. Thus, while this is likely the case in our study as well, we cannot fully rule out that some degree of selection bias was present. Another limitation was the exclusion of women with insufficient knowledge of the German language, which might affect the vaccination coverage assessed for women with migration background and its relevance as a factor influencing vaccine uptake. However, several other important characteristics such as migration background and the proportion of foreign born individuals were similar to that of the general female population, which is a result of the recruitment strategy, the large study sample, and the weighting procedures. Since no representative national perinatal dataset exists, we
Please cite this article in press as: Bödeker B, et al. Cross-sectional study on factors associated with influenza vaccine uptake and pertussis vaccination status among pregnant women in Germany. Vaccine (2014), http://dx.doi.org/10.1016/j.vaccine.2014.06.007
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compared characteristics of our study sample with that of women of childbearing age living in Germany. In conclusion, STIKO-recommendations related to the protection of pregnant woman and newborns against seasonal influenza and pertussis are not effectively implemented in Germany. Special efforts must be undertaken to enhance influenza vaccine uptake. In this context, especially gynecologists play an important role and should be included as a major target group in communication activities. Both pregnant women and gynecologists need to be adequately informed about risks and benefits of influenza vaccines as well as disease-related risks. Education of physicians and women is also needed to increase the awareness of the current STIKOrecommendations for pertussis vaccination and to underline the importance of being immunized before pregnancy or shortly after delivery to indirectly protect the infant. While pertussis vaccination is currently not part of the antenatal care program in Germany, gynecologists should nonetheless offer pregnant women postnatal pertussis vaccination if not already vaccinated and inform them of the need for timely vaccination of other members of the household to protect infants from pertussis. Monitoring tools should be implemented to investigate vaccination coverage among pregnant women as well as the effectiveness of both interventions. Contributions All authors were involved in the conception and design of the study. BB performed the data analysis and drafted the article. All authors contributed to the data interpretation and finalization of the manuscript. Conflict of interest The authors have declared no conflicts of interest. Acknowledgments
We would like to thank all pregnant women who participated in the study and Wiebke Hellenbrand (RKI) who provide important 447 Q2 input in the discussions around pertussis. The study was funded by 448 Q3 the Federal Ministry of Health. 449 446
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