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Human Vaccines & Immunotherapeutics Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/khvi20
Knowledge, attitude, and uptake related to human papillomavirus vaccination among young women in Germany recruited via a social media site a
a
b
b
Cornelius Remschmidt , Dietmar Walter , Patrick Schmich , Matthias Wetzstein , Yvonne a
Deleré & Ole Wichmann a
a
Immunization Unit; Robert Koch Institute; Berlin, Germany
b
Health Monitoring: Surveys and European Cooperation Unit; Robert Koch Institute; Berlin, Germany Published online: 30 Oct 2014.
Click for updates To cite this article: Cornelius Remschmidt, Dietmar Walter, Patrick Schmich, Matthias Wetzstein, Yvonne Deleré & Ole Wichmann (2014) Knowledge, attitude, and uptake related to human papillomavirus vaccination among young women in Germany recruited via a social media site, Human Vaccines & Immunotherapeutics, 10:9, 2527-2535, DOI: 10.4161/21645515.2014.970920 To link to this article: http://dx.doi.org/10.4161/21645515.2014.970920
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RESEARCH PAPER Human Vaccines & Immunotherapeutics 10:9, 2527--2535; September 2014; © 2014 Taylor & Francis Group, LLC
Knowledge, attitude, and uptake related to human papillomavirus vaccination among young women in Germany recruited via a social media site Cornelius Remschmidt1,y,*, Dietmar Walter1,y, Patrick Schmich2, Matthias Wetzstein2, Yvonne Delere1, and Ole Wichmann1 1
Immunization Unit; Robert Koch Institute; Berlin, Germany; 2Health Monitoring: Surveys and European Cooperation Unit; Robert Koch Institute; Berlin, Germany y
These authors contributed equally to this work.
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Keywords: human papillomavirus, cross-sectional study, recruitment strategy, social media site, targeting advertisement, uptake, vaccine Abbreviations: HPV, human papillomavirus; hr, high-risk; CI, confidence interval; OR, odds ratio.
Background: Many industrialized countries have introduced human papillomavirus (HPV) vaccination of young women, but vaccine uptake often remains suboptimal. This study aimed to investigate whether a social media site like Facebook is an appropriate tool to assess knowledge, attitude and uptake related to HPV vaccination in young women in Germany. Methods: Between December 2012 and January 2013 two different targeting strategies were implemented on Facebook, providing a link to an online questionnaire. Advertisements were displayed to female Facebook users aged 18–25 years living in Germany. During the simple targeting strategy, advertisements comprised health-related images along with various short titles and text messages. During the focused strategy, advertisements were targeted to users who in addition had certain fashion brands or pop stars listed on their profiles. The targeting strategies were compared with respect to participant characteristics. Univariate and multivariate analyses were used to identify factors associated with HPV vaccine uptake. Results: A total of 1161 women participated. The two targeting strategies resulted in significant differences regarding educational status and migrant background. Overall, awareness of HPV was high, but only 53% received at least one vaccine dose. In multivariate analysis, HPV vaccine uptake was independently associated with a physician’s recommendation and trust in vaccine effectiveness. Concerns of adverse effects were negatively associated with vaccine uptake. Discussion: Social network recruitment permits fast and convenient access to young people. Sample characteristics can be manipulated by adjusting targeting strategies. There is further need for promoting knowledge of HPV vaccination among young women. Physicians have a major role in the vaccination decision-making process of young women.
Introduction Human papillomavirus (HPV) infections are among the most common sexually transmitted diseases worldwide.1 Persistent infections with high-risk (hr) HPV types can lead to cervical cancer.2 Two vaccines targeting hr HPV types 16 and 18 are available, and immunization against HPV has been recommended in Germany since 2007, and is free of charge to all females aged 12–17 y.3 Despite the high prevalence of hr HPV types in sexually active women and convincing evidence of the safety and effectiveness of the HPV vaccine,4-8 surveys indicated
unsatisfactorily low vaccination coverage in the target age group in Germany, ranging from 41% to 49%.9,10 Since a comprehensive program for HPV vaccine administration and evaluation is lacking in Germany, data on HPV vaccination coverage are not routinely available. In addition to coverage data, an understanding of barriers and facilitators related to HPV vaccination is crucial to guide communication strategies and to eventually improve acceptance of the vaccine and vaccination coverage. In many industrialized countries, barriers and facilitators to HPV vaccination in young women have been found to be multifactorial.9-11 While concerns regarding vaccine safety and
*Correspondence to: Cornelius Remschmidt; Email: [email protected] Submitted: 03/19/2014; Revised: 05/19/2014; Accepted: 06/10/2014 http://dx.doi.org/10.4161/21645515.2014.970920
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efficacy were among the most commonly reported barriers, facilitators included greater vaccine-related knowledge and perceived benefits of vaccination. In Germany, such an assessment of barriers and enablers of HPV vaccination has so far only been performed among school students in Berlin.9,12 Recruitment of young people into health research is challenging. However, since approximately 80% of persons aged 14–29 y are using social networks, and Facebook in particular,13,14 recruiting via this social network site might be a promising and inexpensive strategy. In fact, Facebook has already been used in different research settings,15 and advertising has been shown to be effective in reaching young women14 or addressing sensitive topics.16,17 Recently, Gunasekaran et al. conducted a survey on HPV knowledge among young women in Australia using targeted advertising on Facebook as a recruitment strategy.18 The primary aim of our study was to assess the strategy of recruiting young females in Germany via a social media site and to explore the impact of different targeting strategies on study sample characteristics. Secondary aims were to assess awareness, knowledge, and attitude related to HPV-infection and HPV vaccine uptake and to identify factors associated with receipt of the HPV vaccine and completion of the HPV vaccination series.
Results Recruitment and participation The study advertisements (n D 39) were viewed 62 928 542 times on Facebook (Fig. 1). Twenty-one different Total views on facebook 62,928,542
Total views in phase 1 35,225,854
Total views in phase 2 27,702,688
Clicks on ad in phase 1 n=5,897 (Click-Through-Rate: 0.017%)
Clicks on ad in phase 2 n=7,136 (Click-Through-Rate: 0.026%)
Starts of survey in phase 1 n=568
Starts of survey in phase 2 n=826
Completed survey in phase 1 n=494 (Conversion-Rate: 8.4%)
Completed survey in phase 2 n=667 (Conversion-Rate: 9.3%)
Figure 1. Performance of targeting strategy by paid ads in a social network shown in total and by study phase, Germany 2012–13.
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advertisements were shown during phase one when the “simple targeting strategy” was applied, and 18 during phase two during the “focused targeting strategy.” The highest number of total daily views was 4 million. The most frequently shown advertisement had a total of 3.3 million views (for examples see Supplemental Materials). In the first phase 5897 and in the second phase 7136 women clicked on the advertisements. The total click-through-rate was 0.021%. A total of 1161 women completed the questionnaire. The overall dropout rate after starting the questionnaire was 16.4%, and the conversion rate was 8.9%. We observed differences in characteristics of participants after the simple targeting strategy in the first study phase compared with participants after focused targeting in the second phase (Table 1). Focused targeting resulted in the recruitment of younger women, more women from East Germany, more women with a migrant background, and more participants with a lower educational status. However, we did not observe statistically significant differences between the study phases with respect to the population of the district of residence or relevant outcome variables such as HPV vaccination coverage or behavioral factors. Risk perception The perceived likelihood of ever developing cervical cancer and of ever being treated for cervical precancerous lesions was 26.8% (SD § 0.7%) and 30.8% (SD § 0.7%), respectively. In the final multivariable linear model the perceived risk of developing cervical cancer significantly decreased with higher education, being HPV-vaccinated, and older age at first intercourse; it increased with higher age (data not shown). HPV awareness, knowledge, and attitude Overall, 1116 (96.1%; 95% confidence interval [CI], 94.8–97.2%) stated that they had heard of the HPV vaccine. Of these, 617 (55.3%) felt “very well” or “well,” 423 (37.9%) “less well,” and 76 (6.8%) “poorly” informed about the HPV vaccine. With respect to vaccines in general, 699 (62.6%; 95%CI, 59.7– 65.5%) women stated they had actively sought this information previously in their life. The most commonly utilized information sources were physicians (“frequently” consulted in 36.0%) followed by parents (27.0%), whereas “school” was the least important source and consulted “frequently” by only 13.7%. Differences between HPV unvaccinated and vaccinated women were statistically significant regarding all attitude and knowledge items (P < 0.01 for all, Table 2). For example, a higher proportion of vaccinated women were convinced of the effectiveness of the vaccine compared with unvaccinated women (88.9% vs. 67.8% “strongly,” “somewhat,” or “slightly” agreed). Furthermore, only 3.4% of vaccinated women “strongly” agreed that HPV vaccines had severe side effects, while this was the case in 17.1% of unvaccinated women. With regard to knowledge items, a larger proportion of HPV-vaccinated women knew that HPV vaccination cannot replace cervical cancer screening and that condom use alone does not sufficiently protect against HPV infection.
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Table 1. Baseline characteristics of the total female population aged 18–25, the study population (n D 1,161), and differences between study phase one (n D 494) and two (n D 667), Germany 2012—13 German population1 (18–25 y), 2012
Study population (n D 1,161)
First Phase (n D 494)
Second Phase (n D 667)
%
n2 (%)
n2 (%)
n2 (%)
22.1 37.9 40.0
415 (35.8) 447 (38.5) 229 (25.7)
162 (32.8) 186 (37.7) 146 (29.5)
253 (37.9) 261 (39.2) 153 (22.9)
35.8 28.0 18.1 18.1
375 (36.3) 292 (28.3) 185 (17.9) 180 (17.5)
153 (33.9) 137 (30.4) 85 (18.9) 76 (16.8)
222 (38.2) 155 (26.7) 100 (17.2) 104 (17.9)
18.8 81.2
243 (21.0) 916 (79.0)
89 (18.0) 404 (82.0)
154 (23.1) 512 (76.9)
77.1 22.9
875 (75.4) 286 (24.6)
427 (86.4) 67 (13.6)
448 (67.2) 219 (32.8)
59.0 41.0
373 (33.4) 728 (65.5)
101 (21.4) 372 (78.6)
247 (39.1) 385 (60.9)
729 (62.9) 73 (6.3) 19 (1.7) 338 (29.2)
317 (64.4) 4 (0.8) 10 (2.0) 161 (32.8)
412 (61.8) 69 (10.3) 9 (1.4) 188 (26.5)
183 (15.8) 555 (48.1) 252 (21.8) 165 (14.3)
70 (14.3) 242 (49.5) 121 (24.7) 56 (11.5)
113 (17.0) 313 (47.0) 131 (19.7) 109 (16.3)
516 (46.2) 595 (53.3) 6 (0.5)
222 (46.4) 255 (53.4) 1 (0.2)
294 (46.0) 340 (53.2) 5 (0.8)
151 (25.4) 444 (74.6)
60 (23.5) 195 (46.5)
91 (26.8) 249 (73.2)
30 (2.6) 1049 (90.3) 82 (7.1)
7 (1.4) 450 (91.1) 37 (7.5)
23 (3.5) 599 (89.8) 45 (6.7)
Variable/Category Age (years)3 18–19 20–22 23–25 Size of residency (inhabitants) < 20,000 20,000–100,000 > 100,000–500,000 > 500,000 Region of residency3 Eastern federal states Western federal states Migrant background3 No Yes Education3 Less than university access degree or still in education University access degree Religion3 Christian Islamic other none Age at first intercourse (years)3 14 15–16 17 not yet Vaccinated against HPV (at least one dose) No Yes Don’t know Completion of HPV vaccination series No Yes Vaccinated against tetanus No Yes Don’t know 1
Federal Statistical Office of Germany, Mikrozensus 2011 (if available); between first and second phase (chi-square test).
2
Numbers may not add up to the total number owing to missing data;
HPV-vaccination Overall, 595 (53.3%; 95%CI, 50.3–56.3%) participants were vaccinated against HPV, and 516 (46.3%; 95%CI, 43.3–49.1%) were not. In the final multivariate model, HPV vaccine uptake of at least one dose was independently associated with a physician’s recommendation and belief of vaccine effectiveness; it was negatively associated with an increase in age, concerns of severe side effects, and with the misconception that condoms adequately protect against HPV infection (Table 3). Among the 595 vaccinated women, 444 (74.6%; 95%CI, 70.9–78.1%) received the full three-dose course. Completion of HPV vaccination was independently associated with women who felt very well or well informed about HPV vaccines (OR, 2.1; 95%CI, 1.2–2.7), and
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3
P < 0.05
who had a higher educational background (OR, 1.7; 95%CI, 1.1–2.9). The most commonly stated reasons for not having received the vaccine were the receipt of recommendations against the vaccination (n D 206/516 [39%], most frequently by family members [n D 54 {10%}], physicians [n D 45 {9%}], and friends [n D 46 {9%}]); a negative experience with vaccinations in general [n D 89 {17.2%}]), and fear of injections (n D 75 [14.5%]). Forty-nine (9.5%) women reported that they were not aware of the HPV vaccine. Time of HPV-vaccination with regard to sexual debut Overall, 355 (59.7%) participants provided information on time of vaccination (first dose) and age at first intercourse; 186
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Table 2. Responses to attitude and knowledge items among unvaccinated (n D 516) and vaccinated (n D 595) women, Germany 2012—13
I am convinced of the effectiveness of the HPV-vaccine Vaccination against HPV has strong side effects
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I felt sufficiently informed to opt for or against HPV-vaccination Vaccination against HPV replaces the need for cervical cancer screening Since condoms protect sufficiently against infection, HPV vaccination is not necessary
Vaccination status
Strongly agree (%)
Somewhat agree (%)
Slightly agree (%)
Do not agree (%)
Do not know (%)
p-value
unvaccinated vaccinated unvaccinated vaccinated unvaccinated vaccinated unvaccinated vaccinated unvaccinated vaccinated
8.9 32.4 17.1 3.4 20.0 37.7 2.1 1.5 1.6 0.2
31.2 47.6 19.4 8.7 21.1 32.3 4.3 2.3 6.6 1.8
27.7 8.9 9.9 16.5 19.8 17.0 9.1 10.2 17.4 6.9
16.5 2.5 4.1 64.7 29.3 9.9 66.9 76.5 52.5 86.2
16.7 8.6 49.6 6.7 9.0 3.5 17.6 9.4 21.9 4.9
— < 0.01 — < 0.01 — < 0.01 — < 0.01 — < 0.01
(52.4%) received the first dose before sexual debut. This proportion decreased with an increase in age at time of vaccination (Fig. 2). For example at the age of 17 y, more than 60% had already had sexual intercourse.
Discussion Our study demonstrated the feasibility of recruiting young women into health research via a social networking site in Germany. Different targeting strategies optimized the composition of the study population with respect to the proportion of lower educated women and those with a migrant background, groups which are often underrepresented in self-selected samples. Over 90% of participants were aware of HPV. Self-reported HPV vaccination coverage was 53%, and uptake was independently associated with a physician’s recommendation and knowledge of HPV vaccine effectiveness and safety. Previous studies found that social networks are a useful tool to recruit young persons, even when addressing sensitive research questions.14-17 The anonymity guaranteed by online surveys are of benefit if study topics are personal or taboo, such as questions on sexuality as in the case of HPV, where household or schoolbased recruitment strategies may be less favorable.16,17 Recently, a study used Facebook to collect data on knowledge of HPV and cervical cancer among young women in Australia.18 In that study, characteristics of the study population did not differ from data from the National Bureau of Statistics with regard to geographic region, ethnicity and socioeconomic status; however, women aged 16–17 y and those with higher education were underrepresented. Samples recruited from social media networks tend to have an overrepresentation of females and younger adults.15 One study, which compared traditional with online advertisement recruitment found that men, young adults, ethnic minorities, and a high school education or less were more likely to be recruited via online advertizing.19 In the current study, we were able to adjust the targeting strategy based on an interim analysis of key characteristics, thereby optimizing the study sample composition; the focused targeting strategy applied during the second phase was successful in increasing the proportion of lower educated women and women with a migrant background.
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However, despite optimizing the targeting strategy, we observed a loss of potential participants during the click-through process until the start of the questionnaire, and still recruited a higher proportion of women with a higher education status compared with the general German female population. Keeping the advertisement neutral in appearance and text (i.e., health-related advertisements without an obvious link to vaccine-related subjects) may limit selection to those likely to have an interest in HPV vaccination. Overall, Facebook provided an easy means of contact with young women in Germany. The targeting strategies in our study were developed in cooperation with a company specialized in this field. Facebook provides access to online tools to create targeting advertisements, but for those not working in this field, it requires some time to get familiar with these tools. The average perceived likelihood of developing cervical cancer was low at 27% in our population, and was smaller in those with higher educational attainment and who had received the HPV vaccine. One study conducted in Italy prior to the introduction of HPV vaccines found that women who perceived they had a high risk of contracting HPV infection were more likely to receive the vaccine in the future.20 In contrast, in our study, women with a higher perceived risk of being treated for cervical cancer in the future had a lower chance of being vaccinated against HPV, although in multivariate analysis this was not statistically significant (data not shown). A possible explanation is that our study was conducted after introduction of the HPV vaccine in the population. Women who were already been vaccinated against HPV might have had an even higher perceived risk before vaccination (which initiated the decision), and the perceived risk of developing HPV-related disease decreased after receiving the vaccination. Regarding attitude and knowledge items, vaccinated women were more often convinced of the effectiveness of the vaccine and were less often concerned about side effects. Two recently published reviews found that doubts about vaccine effectiveness, concerns of safety, and fear of side effects were among the most common themes related to HPV vaccine uptake.11,21 Knowledge regarding HPV has been shown to be relatively low in various settings,21-23 although it has increased since introduction of HPV vaccines.24 In our study, 76.5% and 66.9% of vaccinated and unvaccinated women knew that HPV vaccination cannot replace
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Table 3. Factors potentially associated with HPV-vaccine uptake among 1,161 females aged 18–25 y, Germany 2012–13
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Variable/Category Age (years) 18–19 20–22 23–25 Region of residency Eastern federal states Western federal states Migrant background No Yes Education Less than university access degree or still in education University access degree Religion Christian Islamic other none HPV-vaccination recommended by physician No Yes Vaccinated against tetanus No Yes Level of being informed about HPV vaccines less well/ poorly informed Very well/well informed Actively sought information on HPV vaccination No Yes Convinced of HPV vaccine effectiveness No1 Yes2 Concerns of HPV vaccine severe side effects No1 Yes2 Feels adequately informed to opt for/against HPV vaccination No1 Yes2 Opinion that HPV-vaccination replaces cervical cancer screening No1 Yes2 Opinion that condoms protect against HPV, thus vaccination is not necessary No1 Yes2
HPV vaccination coverage (%)
Crude OR (95% CI)
Adjusted OR (95% CI)
61.6 62.5 27.5
1 1.0 (0.8–1.4) 0.2 (0.2–0.3)
1 1.2 (0.7–2.1) 0.5 (0.2–1.0)
59.2 51.9
1 0.7 (0.5–1.0)
ns
54.3 51.2
1 0.4 (0.7–1.2)
ns
48.9 55.6
1 1.3 (1.0–1.6)
ns
55.8 57.1 41.2 48.8
1 1.1 (0.6–1.8) 0.6 (0.2–1.5) 0.8 (0.6–1.0)
ns
10.6 78.0
1 29.9 (20.2–44.4)
1 33.3 (15.6–70.7)
18.5 54.9
1 5.4 (2.0–14.2)
ns
35.0 68.4
1 4.0 (3.1–5.2)
ns
37.4 62.9
1 2.8 (2.2–3.6)
ns
15.0 60.5
1 8.7 (4.9–15.3)
1 4.0 (1.5–10.8)
94.0 41.6
1 0.04 (0.03–0.1)
1 0.03 (0.01–0.06)
28.1 62.1
1 4.2 (3.0–5.8)
ns
56.9 51.2
1 0.8 (0.6–1.1)
ns
65.4 28.6
1 0.2 (0.1–0.3)
1 0.2 (0.1–0.4)
95% CI, 95% confidence interval; OR, odds ratio; ns, statistically not significant; 1 “I do not agree”; 2 “I strongly/somewhat/slightly agree.”
regular cervical cancer screening. However, 15% of the entire study population did at least “slightly agree” with that item, revealing the need for educational interventions to improve the level of knowledge about HPV transmission routes and prevention of HPV-related diseases. We found an HPV vaccination coverage of 53%, which is comparable to results (49%) of a telephone survey among 18–20-y-old females conducted in Germany in 2010.10 In agreement with findings of other studies, HPV vaccine uptake was strongly associated with a vaccination recommendation from a physician. Although a study in the Netherlands showed the complexity of the decision-making process as to whether or not to be
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vaccinated against HPV,25 a primary healthcare provider played a crucial role in initiating or completing the vaccine course, at least in settings where structured (e.g., school-based) vaccination programs did not exist.26,27 Only 11% of women in our study who had no doctor’s recommendation received the HPV vaccine compared with 80% of those who were advised to have the vaccination. This highlights the importance of physicians in influencing an individual’s decision-making process to receive the vaccine.28 Positive attitudes of physicians toward the HPV vaccine have been shown to be the main driving force in vaccine uptake, whereas the option was hindered by perceived parental or girls concerns regarding safety and side effects.21,28,29
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Figure 2. Proportion of women vaccinated before (light gray bars) and after (dark gray bars) sexual debut, Germany 2012–13 (n D 355).
In our study, less than 4% of women reported that they were advised against HPV vaccination by a physician. A more detailed analysis regarding specialization or residency of those physicians was not possible since this information was not assessed in the questionnaire. When time of HPV vaccination with regard to sexual debut is interpreted, the age of study participants and endorsement date of the recommendation for HPV vaccination have to be taken into account. Women aged 25 y at the time of our study were 20 y old when HPV vaccination was adopted into the national immunization schedule in Germany. Therefore, it is not surprising that a large proportion of the women received the vaccine after sexual debut and that this proportion increased with increasing age. Results on age of first sexual intercourse in Germany have been previously assessed by a representative survey on youth sexuality in 2009.30 This study revealed that 53% of women with (our study 69%) and 66% without a migrant background (our study 75%) had experienced their first sexual intercourse at the age of 17. Whether these differences could be explained through the anonymity of our survey can only be assumed since comparison of results are limited owing to differences in study populations and study time. Our study benefits from its innovative design and large sample size, including women from different ethnic and socioeconomic backgrounds across the country. We were able to recruit more than 1000 women of the targeted population in less than 4 wk. Optimizing the targeting strategy, we were able to recruit a study population that resembled more closely the general female population in that age group living in Germany. Nevertheless, some limitations of our study need to be acknowledged. First, we used a cross-sectional design that generally precluded determination of causal relationships between outcomes and potentially relevant factors. Second, younger adolescents were not included, although they are the primary target for HPV vaccination. It is possible
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that HPV-related awareness, knowledge and attitude, and HPV vaccine uptake in the younger age group differs from that in our study population. Third, recruiting via a social network itself and the low click-through rate may have introduced selection bias, and thus representativeness of the sample could not be fully determined. Nevertheless, although women with a higher education and younger women were over-represented in our study, several important characteristics of our study sample were comparable to the general female population in Germany. Fourth, information on sexual behavior, vaccination status, and other characteristics was self-reported and could be subject to misclassification. Fifth, it could not be validated whether the stated age and other characteristics of the participant Facebook accounts were correct. Finally, repeated participation in the survey could not be ruled out and might have biased both the demographics of the study population and the results regarding HPV vaccine-related issues. However, providing a valid e-mail address for the lottery draw and excluding participants who completed the questionnaire in a very short time should have reduced this possibility. These limitations have to be borne in mind when the results on HPV vaccine-related knowledge, attitudes and uptake are compared with data using traditional recruitment methods. In conclusion, we were able to show that social media networks can be used as a recruitment tool for health-related online surveys among adolescents and young adults. In addition, study sample composition can be manipulated by applying adjusted or more focused targeting strategies. Given the increasing number of Facebook users in this age group, recruiting via this networking site has the potential to achieve large samples of representative surveys within a short time period. Results on HPV vaccinerelated knowledge, attitudes and uptake were comparable to results of studies using traditional recruitment methods, and indicated a further need for promotion of knowledge of HPVvaccines in terms of benefit and harm among young women. In addition, physicians should be aware of their important role in the decision-making process to opt for or against HPV vaccination when discussing this issue with their young patients.
Methods Advertising on Facebook Use of Facebook requires initial registration using a valid e-mail address. After log-in, the user can adapt her/his profile and add personal data, such as place of residence, gender, age, or personal interests. These data—if not hidden via the privacy settings of Facebook—can be used by third parties for paid targeted advertisements to reach people with interests that are similar to the products offered or products that are gender-specific (https:// www.facebook.com/business/products/ads). These advertisement strategies can be simple, such as targeting a large group of people (e.g., advertisements are displayed to all women living in Germany), or focused, when more specific targeting options are used (e.g., advertisements are displayed to women aged 18–25 y living in Germany, to Turkish-speaking users, to those with an interest in a certain pop star). After implementation, performance of the
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targeting strategy can be monitored using the so-called “ads manager.” This online tool provides data on total views of the advertisement (i.e., number of times it has been shown to a targeted user), the number of clicks on it, the click-through-rate (the number of clicks on an advertisement divided by the number of times it has been viewed), and the conversion rate (the proportion of visitors on the study website who completed the questionnaire). Targeting strategy Inclusion criteria for participation were (1) female gender, (2) age 18–25 y, and (3) resident in Germany. The age group was chosen since these women already had decided for or against HPV vaccination (HPV vaccination in Germany is free of charge only between 12 and 17 y of age). In addition, for legal reasons, females younger than 18 y were not permitted to participate in the lottery draw, vouchers for which were used as an incentive to complete the questionnaire in the current study. Between December 2012 and January 2013, paid advertisements were shown on Facebook to recruit eligible women for an online survey related to HPV immunization in Germany. The targeting strategy was developed in cooperation with a company specialized in online display advertising and landing page optimization. In the first study phase (10–23 December 2012) we applied a simple strategy. The advertisements comprised an image (e.g., showing young women of various ethnic backgrounds, female physicians, or health-related symbols such as a stethoscope) combined with variations of short titles (e.g., “Your participation is needed”) and short text messages (e.g., “Take part in a survey of the Robert Koch Institute”) and were displayed to Facebook users if they identified themselves as female, age 18–25 y, and living in Germany. Some examples of advertisements utilized in this study can be found in the Supplemental Materials. In the second study phase (8–17 January 2013) we applied a focused targeting strategy, which was guided by results of an interim analysis of the first study phase, by adding one additional target set: advertisements were displayed to Facebook users who additionally had certain fashion brands, rap stars, TV series, or TV channels listed on their profile. The interim analysis had indicated that women who were migrants were underrepresented in the first study phase, so we also included a target set of Turkish TV or pop stars and different languages (e.g., Polish, Russian, or Turkish) for relevant migrant groups in Germany to increase the participation rate of this group. However, as with the simple targeting strategy, titles and text messages as well as the questionnaire were provided in the German language only. There were 39 different advertisements (21 in phase one and 18 in phase two) during the study period. By clicking on the advertisements, women were directed to the landing page of the survey website, which provided information on the study aims and background. As an incentive, vouchers for an online lottery draw worth €20 each were promised to participants who gave their email address at the end of the questionnaire. Questionnaire We used a structured questionnaire consisting of 26 questions in the German language to collect information on (1) HPV
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awareness, (2) knowledge, attitude, and behavior related to HPV immunization, as well as (3) sociodemographic factors. At the beginning of the survey, participants were asked to rate their perceived likelihood of ever (1) developing cervical cancer or (2) being treated for cervical precancerous lesions (response scale 0–100%) and whether they “have ever heard of the HPV vaccine” (response options: “Yes,” “No,” “Don’t know”). Women who had heard of the vaccine were then asked how well informed they felt about the vaccine (“very well,” “well, “less well,” “poorly” informed). Their attitude toward and knowledge of HPV vaccines was assessed by providing five-point Likert scale response options (“I strongly agree,” “I somewhat agree,” “I slightly agree,” “I do not agree,” and “I don’t know”) to the following questions: “I am convinced of the effectiveness of the HPV-vaccine,” “Vaccination against HPV has severe side effects,” “I felt sufficiently informed to opt for or against HPV vaccination,” “Vaccination against HPV replaces the need for cervical cancer screening,” and “Since condoms protect sufficiently against infection, HPV-vaccination is not necessary.” In addition, women were asked whether they had actively sought information about vaccinations in general (“Yes,” “No,” “Don’t know”), and if “Yes” how often, and which type of information source (e.g., physician, parents, school, internet, etc.) was consulted most frequently. Regarding receipt of the HPV vaccine, participants were asked whether the vaccine was recommended by a physician and whether they had finally received the vaccine (“Yes,” “No,” “Don’t know”). However, women were not asked where the vaccination took place. Unvaccinated women were in addition asked the reasons for not being vaccinated, with the option of multiple answers. In addition, participants were asked to report if they were vaccinated against tetanus (“Yes,” “No,” “Don’t know”). Finally, sociodemographic data were collected, such as age (years/ month), age at first intercourse (years), immigration status (i.e., at least one parent was an immigrant into Germany), place of residence, level of school education, and religion (Christian, Muslim, other, none). Voxco Survey Software was used for programming and management of the online survey. Data from the questionnaires were self-reported and not validated. Ethical considerations Participation in the study was only possible after agreement to a consent form. The questionnaire was anonymous. Emails for the lottery draw were technically separated from the data of the questionnaire. Women had to be at least 18 y to participate in the study. The study was approved by the German Federal Commissioner for Data Protection and Freedom of Information. Repeated participation Owing to the anonymity of the survey and according to the approval by the German Federal Commissioner for Data Protection and Freedom of Information, the Internet Protocol (IP) address of participants were not saved or tracked. Although women were informed that participation in the study was possible only once, repeated participation could therefore not be ruled out. However, a valid e-mail address was required for the lottery
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draw, and participants who completed the questionnaire in a very short time (defined as 0.8), multiple linear regression was conducted only for linear model 1. To identify independent predictors of HPV vaccine uptake (at least one dose) and completion of the HPV vaccination series, we used univariate analyses for all binary or categorical exposure variables and calculated the crude odds ratios (OR) and 95% confidence intervals (CI). For the purpose of univariate and multivariate logistic regression, data on knowledge were collapsed into two categories “Strongly/somewhat/slightly agree” vs. “I do not agree.” Participants who answered “I do not know” were excluded from the analysis. Variables with a P value < 0.1 in the univariate analysis were included in the initial step for multivariate logistic regression modeling, followed by stepwise backward References 1. Veldhuijzen NJ, Snijders PJ, Reiss P, Meijer CJ, van de Wijgert JH. Factors affecting transmission of mucosal human papillomavirus. Lancet Infect Dis 2010; 10:862–74; PMID:21075056; http://dx.doi.org/ 10.1016/S1473-3099(10)70190-0 2. Schiffman M, Castle PE, Jeronimo J, Rodriguez AC, Wacholder S. Human papillomavirus and cervical cancer. Lancet 2007; 370:890–907; PMID:17826171; http://dx. doi.org/10.1016/S0140-6736(07)61416-0 3. Delere Y, Meyer C, Reiter S. Universal immunisation with human papillomavirus (HPV) vaccine among females aged 12-17 recommended in Germany. Euro Surveill 2007; 12:E070405.2; PMID:17439800 4. Kjaer SK, Breugelmans G, Munk C, Junge J, Watson M, Iftner T. Population-based prevalence, type- and age-specific distribution of HPV in women before introduction of an HPV-vaccination program in Denmark. Int J Cancer 2008; 123:1864–70; PMID:18661520; http://dx.doi. org/10.1002/ijc.23712 5. Iftner T, Eberle S, Iftner A, Holz B, Banik N, Quint W, Straube AN. Prevalence of low-risk and high-risk types of human papillomavirus and other risk factors for HPV infection in Germany within different age groups in women up to 30 years of age: an epidemiological observational study. J Med Virol 2010; 82:1928–39; PMID:20872721; http://dx.doi.org/10.1002/jmv.21910 6. Delere Y, Remschmidt C, Leuschner J, Schuster M, Fesenfeld M, Schneider A, Wichmann O, Kaufmann AM. Human Papillomavirus prevalence and probable first effects of vaccination in 20 to 25 year-old women in Germany: a population-based cross-sectional study via home-based self-sampling. BMC Infect Dis 2014; 14:87; PMID:24552260; http://dx.doi.org/10.1186/ 1471-2334-14-87 7. Lehtinen M, Paavonen J, Wheeler CM, Jaisamrarn U, Garland SM, Castellsague X, Skinner SR, Apter D,
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removal of all variables with a P value > 0.05 to obtain the final model. Two-sided hypothesis tests were performed, and a P value < 0.05 was considered statistically significant. Missing data were treated as such and not imputed. The statistical software package STATAÒ , version 11 (STATA Corp.) was used. Disclosure of Potential Conflicts of Interest
No potential conflicts of interest were disclosed. Acknowledgments
We would like to thank all the women who participated in the study. Funding
The study was funded by internal funds of the Robert Koch Institute. Contributions
All authors were involved in the conception and design of the study. C.R. performed the data analysis and drafted the article. All authors contributed to data interpretation and the final version of the manuscript. Supplemental Materials
Supplemental materials may be found here: landesbioscience.com/journals/vaccines/article/29541/
Naud P, Salmeron J, et al.; HPV PATRICIA Study Group. Overall efficacy of HPV-16/18 AS04-adjuvanted vaccine against grade 3 or greater cervical intraepithelial neoplasia: 4-year end-of-study analysis of the randomised, double-blind PATRICIA trial. Lancet Oncol 2012; 13:89–99; PMID:22075171; http://dx. doi.org/10.1016/S1470-2045(11)70286-8 Paavonen J, Naud P, Salmeron J, Wheeler CM, Chow SN, Apter D, Kitchener H, Castellsague X, Teixeira JC, Skinner SR, et al.; HPV PATRICIA Study Group. Efficacy of human papillomavirus (HPV)-16/18 AS04-adjuvanted vaccine against cervical infection and precancer caused by oncogenic HPV types (PATRICIA): final analysis of a double-blind, randomised study in young women. Lancet 2009; 374:301–14; PMID:19586656; http://dx.doi.org/ 10.1016/S0140-6736(09)61248-4 St€ocker P, Dehnert M, Schuster M, Wichmann O, Delere Y. Human papillomavirus vaccine uptake, knowledge and attitude among 10th grade students in Berlin, Germany, 2010. Hum Vaccin Immunother 2013; 9:74–82; PMID:22995838; http://dx.doi.org/ 10.4161/hv.22192 Delere Y, B€ohmer MM, Walter D, Wichmann O. HPV vaccination coverage among women aged 1820 years in Germany three years after recommendation of HPV vaccination for adolescent girls: results from a cross-sectional survey. Hum Vaccin Immunother 2013; 9:1706–11; PMID:23732901; http://dx.doi.org/ 10.4161/hv.24904 Rambout L, Tashkandi M, Hopkins L, Tricco AC. Self-reported barriers and facilitators to preventive human papillomavirus vaccination among adolescent girls and young women: a systematic review. Prev Med 2014; 58:22–32; PMID:24176938; http://dx.doi.org/ 10.1016/j.ypmed.2013.10.009 Bl€odt S, Holmberg C, M€uller-Nordhorn J, Rieckmann N. Human Papillomavirus awareness, knowledge and
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23. Agius PA, Pitts MK, Smith AM, Mitchell A. Human papillomavirus and cervical cancer: Gardasil vaccination status and knowledge amongst a nationally representative sample of Australian secondary school students. Vaccine 2010; 28:4416–22; PMID:20434543; http://dx.doi.org/ 10.1016/j.vaccine.2010.04.038 24. Klug SJ, Hukelmann M, Blettner M. Knowledge about infection with human papillomavirus: a systematic review. Prev Med 2008; 46:87–98; PMID:17942147; http://dx.doi.org/10.1016/j.ypmed.2007.09.003 25. Rondy M, van Lier A, van de Kassteele J, Rust L, de Melker H. Determinants for HPV vaccine uptake in the Netherlands: A multilevel study. Vaccine 2010; 28:2070–5; PMID:20045095; http://dx.doi.org/ 10.1016/j.vaccine.2009.12.042 26. Kessels SJ, Marshall HS, Watson M, Braunack-Mayer AJ, Reuzel R, Tooher RL. Factors associated with HPV vaccine uptake in teenage girls: a systematic review. Vaccine 2012; 30:3546–56; PMID:22480928; http://dx.doi.org/ 10.1016/j.vaccine.2012.03.063 27. Sturm LA, Mays RM, Zimet GD. Parental beliefs and decision making about child and adolescent
immunization: from polio to sexually transmitted infections. J Dev Behav Pediatr 2005; 26:441–52; PMID:16344662; http://dx.doi.org/10.1097/00004703200512000-00009 28. Wong MC, Lee A, Ngai KL, Chor JC, Chan PK. Knowledge, attitude, practice and barriers on vaccination against human papillomavirus infection: a crosssectional study among primary care physicians in Hong Kong. PLoS One 2013; 8:e71827; PMID:23990994; http://dx.doi.org/10.1371/journal.pone.0071827 29. Ogilvie GS, Remple VP, Marra F, McNeil SA, Naus M, Pielak KL, Ehlen TG, Dobson SR, Money DM, Patrick DM. Parental intention to have daughters receive the human papillomavirus vaccine. CMAJ 2007; 177:1506– 12; PMID:18056599; http://dx.doi.org/10.1503/ cmaj.071022 30. Bundeszentrale f€ ur gesundheitliche Aufkl€arung (BZgA). Youth Sexuality. Repeat Survey of 14 to 17-year-olds and their parents– current focus: migration – 2010. http:// publikationen.sexualaufklaerung.de/cgi-sub/fetch.php? id=687. Accessed on 30 April 2014. 2010.
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Online advertising to reach and recruit Latino smokers to an internet cessation program: impact and costs. J Med Internet Res 2012; 14:e116; PMID:22954502; http://dx.doi.org/10.2196/jmir.2162 20. Di Giuseppe G, Abbate R, Liguori G, Albano L, Angelillo IF. Human papillomavirus and vaccination: knowledge, attitudes, and behavioural intention in adolescents and young women in Italy. Br J Cancer 2008; 99:225–9; PMID:18628763; http://dx.doi.org/ 10.1038/sj.bjc.6604454 21. Chan ZC, Chan TS, Ng KK, Wong ML. A systematic review of literature about women’s knowledge and attitudes toward human papillomavirus (HPV) vaccination. Public Health Nurs 2012; 29:481–9; PMID:23078419; http://dx.doi.org/10.1111/j.15251446.2012.01022.x 22. Bowyer HL, Marlow LA, Hibbitts S, Pollock KG, Waller J. Knowledge and awareness of HPV and the HPV vaccine among young women in the first routinely vaccinated cohort in England. Vaccine 2013; 31:1051–6; PMID:23277094; http://dx.doi.org/10. 1016/j.vaccine.2012.12.038
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Human Vaccines & Immunotherapeutics Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/khvi20
Knowledge, attitude, and uptake related to human papillomavirus vaccination among young women in Germany recruited via a social media site a
a
b
b
Cornelius Remschmidt , Dietmar Walter , Patrick Schmich , Matthias Wetzstein , Yvonne a
Deleré & Ole Wichmann a
a
Immunization Unit; Robert Koch Institute; Berlin, Germany
b
Health Monitoring: Surveys and European Cooperation Unit; Robert Koch Institute; Berlin, Germany Published online: 30 Oct 2014.
Click for updates To cite this article: Cornelius Remschmidt, Dietmar Walter, Patrick Schmich, Matthias Wetzstein, Yvonne Deleré & Ole Wichmann (2014) Knowledge, attitude, and uptake related to human papillomavirus vaccination among young women in Germany recruited via a social media site, Human Vaccines & Immunotherapeutics, 10:9, 2527-2535, DOI: 10.4161/21645515.2014.970920 To link to this article: http://dx.doi.org/10.4161/21645515.2014.970920
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RESEARCH PAPER Human Vaccines & Immunotherapeutics 10:9, 2527--2535; September 2014; © 2014 Taylor & Francis Group, LLC
Knowledge, attitude, and uptake related to human papillomavirus vaccination among young women in Germany recruited via a social media site Cornelius Remschmidt1,y,*, Dietmar Walter1,y, Patrick Schmich2, Matthias Wetzstein2, Yvonne Delere1, and Ole Wichmann1 1
Immunization Unit; Robert Koch Institute; Berlin, Germany; 2Health Monitoring: Surveys and European Cooperation Unit; Robert Koch Institute; Berlin, Germany y
These authors contributed equally to this work.
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Keywords: human papillomavirus, cross-sectional study, recruitment strategy, social media site, targeting advertisement, uptake, vaccine Abbreviations: HPV, human papillomavirus; hr, high-risk; CI, confidence interval; OR, odds ratio.
Background: Many industrialized countries have introduced human papillomavirus (HPV) vaccination of young women, but vaccine uptake often remains suboptimal. This study aimed to investigate whether a social media site like Facebook is an appropriate tool to assess knowledge, attitude and uptake related to HPV vaccination in young women in Germany. Methods: Between December 2012 and January 2013 two different targeting strategies were implemented on Facebook, providing a link to an online questionnaire. Advertisements were displayed to female Facebook users aged 18–25 years living in Germany. During the simple targeting strategy, advertisements comprised health-related images along with various short titles and text messages. During the focused strategy, advertisements were targeted to users who in addition had certain fashion brands or pop stars listed on their profiles. The targeting strategies were compared with respect to participant characteristics. Univariate and multivariate analyses were used to identify factors associated with HPV vaccine uptake. Results: A total of 1161 women participated. The two targeting strategies resulted in significant differences regarding educational status and migrant background. Overall, awareness of HPV was high, but only 53% received at least one vaccine dose. In multivariate analysis, HPV vaccine uptake was independently associated with a physician’s recommendation and trust in vaccine effectiveness. Concerns of adverse effects were negatively associated with vaccine uptake. Discussion: Social network recruitment permits fast and convenient access to young people. Sample characteristics can be manipulated by adjusting targeting strategies. There is further need for promoting knowledge of HPV vaccination among young women. Physicians have a major role in the vaccination decision-making process of young women.
Introduction Human papillomavirus (HPV) infections are among the most common sexually transmitted diseases worldwide.1 Persistent infections with high-risk (hr) HPV types can lead to cervical cancer.2 Two vaccines targeting hr HPV types 16 and 18 are available, and immunization against HPV has been recommended in Germany since 2007, and is free of charge to all females aged 12–17 y.3 Despite the high prevalence of hr HPV types in sexually active women and convincing evidence of the safety and effectiveness of the HPV vaccine,4-8 surveys indicated
unsatisfactorily low vaccination coverage in the target age group in Germany, ranging from 41% to 49%.9,10 Since a comprehensive program for HPV vaccine administration and evaluation is lacking in Germany, data on HPV vaccination coverage are not routinely available. In addition to coverage data, an understanding of barriers and facilitators related to HPV vaccination is crucial to guide communication strategies and to eventually improve acceptance of the vaccine and vaccination coverage. In many industrialized countries, barriers and facilitators to HPV vaccination in young women have been found to be multifactorial.9-11 While concerns regarding vaccine safety and
*Correspondence to: Cornelius Remschmidt; Email: [email protected] Submitted: 03/19/2014; Revised: 05/19/2014; Accepted: 06/10/2014 http://dx.doi.org/10.4161/21645515.2014.970920
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efficacy were among the most commonly reported barriers, facilitators included greater vaccine-related knowledge and perceived benefits of vaccination. In Germany, such an assessment of barriers and enablers of HPV vaccination has so far only been performed among school students in Berlin.9,12 Recruitment of young people into health research is challenging. However, since approximately 80% of persons aged 14–29 y are using social networks, and Facebook in particular,13,14 recruiting via this social network site might be a promising and inexpensive strategy. In fact, Facebook has already been used in different research settings,15 and advertising has been shown to be effective in reaching young women14 or addressing sensitive topics.16,17 Recently, Gunasekaran et al. conducted a survey on HPV knowledge among young women in Australia using targeted advertising on Facebook as a recruitment strategy.18 The primary aim of our study was to assess the strategy of recruiting young females in Germany via a social media site and to explore the impact of different targeting strategies on study sample characteristics. Secondary aims were to assess awareness, knowledge, and attitude related to HPV-infection and HPV vaccine uptake and to identify factors associated with receipt of the HPV vaccine and completion of the HPV vaccination series.
Results Recruitment and participation The study advertisements (n D 39) were viewed 62 928 542 times on Facebook (Fig. 1). Twenty-one different Total views on facebook 62,928,542
Total views in phase 1 35,225,854
Total views in phase 2 27,702,688
Clicks on ad in phase 1 n=5,897 (Click-Through-Rate: 0.017%)
Clicks on ad in phase 2 n=7,136 (Click-Through-Rate: 0.026%)
Starts of survey in phase 1 n=568
Starts of survey in phase 2 n=826
Completed survey in phase 1 n=494 (Conversion-Rate: 8.4%)
Completed survey in phase 2 n=667 (Conversion-Rate: 9.3%)
Figure 1. Performance of targeting strategy by paid ads in a social network shown in total and by study phase, Germany 2012–13.
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advertisements were shown during phase one when the “simple targeting strategy” was applied, and 18 during phase two during the “focused targeting strategy.” The highest number of total daily views was 4 million. The most frequently shown advertisement had a total of 3.3 million views (for examples see Supplemental Materials). In the first phase 5897 and in the second phase 7136 women clicked on the advertisements. The total click-through-rate was 0.021%. A total of 1161 women completed the questionnaire. The overall dropout rate after starting the questionnaire was 16.4%, and the conversion rate was 8.9%. We observed differences in characteristics of participants after the simple targeting strategy in the first study phase compared with participants after focused targeting in the second phase (Table 1). Focused targeting resulted in the recruitment of younger women, more women from East Germany, more women with a migrant background, and more participants with a lower educational status. However, we did not observe statistically significant differences between the study phases with respect to the population of the district of residence or relevant outcome variables such as HPV vaccination coverage or behavioral factors. Risk perception The perceived likelihood of ever developing cervical cancer and of ever being treated for cervical precancerous lesions was 26.8% (SD § 0.7%) and 30.8% (SD § 0.7%), respectively. In the final multivariable linear model the perceived risk of developing cervical cancer significantly decreased with higher education, being HPV-vaccinated, and older age at first intercourse; it increased with higher age (data not shown). HPV awareness, knowledge, and attitude Overall, 1116 (96.1%; 95% confidence interval [CI], 94.8–97.2%) stated that they had heard of the HPV vaccine. Of these, 617 (55.3%) felt “very well” or “well,” 423 (37.9%) “less well,” and 76 (6.8%) “poorly” informed about the HPV vaccine. With respect to vaccines in general, 699 (62.6%; 95%CI, 59.7– 65.5%) women stated they had actively sought this information previously in their life. The most commonly utilized information sources were physicians (“frequently” consulted in 36.0%) followed by parents (27.0%), whereas “school” was the least important source and consulted “frequently” by only 13.7%. Differences between HPV unvaccinated and vaccinated women were statistically significant regarding all attitude and knowledge items (P < 0.01 for all, Table 2). For example, a higher proportion of vaccinated women were convinced of the effectiveness of the vaccine compared with unvaccinated women (88.9% vs. 67.8% “strongly,” “somewhat,” or “slightly” agreed). Furthermore, only 3.4% of vaccinated women “strongly” agreed that HPV vaccines had severe side effects, while this was the case in 17.1% of unvaccinated women. With regard to knowledge items, a larger proportion of HPV-vaccinated women knew that HPV vaccination cannot replace cervical cancer screening and that condom use alone does not sufficiently protect against HPV infection.
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Table 1. Baseline characteristics of the total female population aged 18–25, the study population (n D 1,161), and differences between study phase one (n D 494) and two (n D 667), Germany 2012—13 German population1 (18–25 y), 2012
Study population (n D 1,161)
First Phase (n D 494)
Second Phase (n D 667)
%
n2 (%)
n2 (%)
n2 (%)
22.1 37.9 40.0
415 (35.8) 447 (38.5) 229 (25.7)
162 (32.8) 186 (37.7) 146 (29.5)
253 (37.9) 261 (39.2) 153 (22.9)
35.8 28.0 18.1 18.1
375 (36.3) 292 (28.3) 185 (17.9) 180 (17.5)
153 (33.9) 137 (30.4) 85 (18.9) 76 (16.8)
222 (38.2) 155 (26.7) 100 (17.2) 104 (17.9)
18.8 81.2
243 (21.0) 916 (79.0)
89 (18.0) 404 (82.0)
154 (23.1) 512 (76.9)
77.1 22.9
875 (75.4) 286 (24.6)
427 (86.4) 67 (13.6)
448 (67.2) 219 (32.8)
59.0 41.0
373 (33.4) 728 (65.5)
101 (21.4) 372 (78.6)
247 (39.1) 385 (60.9)
729 (62.9) 73 (6.3) 19 (1.7) 338 (29.2)
317 (64.4) 4 (0.8) 10 (2.0) 161 (32.8)
412 (61.8) 69 (10.3) 9 (1.4) 188 (26.5)
183 (15.8) 555 (48.1) 252 (21.8) 165 (14.3)
70 (14.3) 242 (49.5) 121 (24.7) 56 (11.5)
113 (17.0) 313 (47.0) 131 (19.7) 109 (16.3)
516 (46.2) 595 (53.3) 6 (0.5)
222 (46.4) 255 (53.4) 1 (0.2)
294 (46.0) 340 (53.2) 5 (0.8)
151 (25.4) 444 (74.6)
60 (23.5) 195 (46.5)
91 (26.8) 249 (73.2)
30 (2.6) 1049 (90.3) 82 (7.1)
7 (1.4) 450 (91.1) 37 (7.5)
23 (3.5) 599 (89.8) 45 (6.7)
Variable/Category Age (years)3 18–19 20–22 23–25 Size of residency (inhabitants) < 20,000 20,000–100,000 > 100,000–500,000 > 500,000 Region of residency3 Eastern federal states Western federal states Migrant background3 No Yes Education3 Less than university access degree or still in education University access degree Religion3 Christian Islamic other none Age at first intercourse (years)3 14 15–16 17 not yet Vaccinated against HPV (at least one dose) No Yes Don’t know Completion of HPV vaccination series No Yes Vaccinated against tetanus No Yes Don’t know 1
Federal Statistical Office of Germany, Mikrozensus 2011 (if available); between first and second phase (chi-square test).
2
Numbers may not add up to the total number owing to missing data;
HPV-vaccination Overall, 595 (53.3%; 95%CI, 50.3–56.3%) participants were vaccinated against HPV, and 516 (46.3%; 95%CI, 43.3–49.1%) were not. In the final multivariate model, HPV vaccine uptake of at least one dose was independently associated with a physician’s recommendation and belief of vaccine effectiveness; it was negatively associated with an increase in age, concerns of severe side effects, and with the misconception that condoms adequately protect against HPV infection (Table 3). Among the 595 vaccinated women, 444 (74.6%; 95%CI, 70.9–78.1%) received the full three-dose course. Completion of HPV vaccination was independently associated with women who felt very well or well informed about HPV vaccines (OR, 2.1; 95%CI, 1.2–2.7), and
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3
P < 0.05
who had a higher educational background (OR, 1.7; 95%CI, 1.1–2.9). The most commonly stated reasons for not having received the vaccine were the receipt of recommendations against the vaccination (n D 206/516 [39%], most frequently by family members [n D 54 {10%}], physicians [n D 45 {9%}], and friends [n D 46 {9%}]); a negative experience with vaccinations in general [n D 89 {17.2%}]), and fear of injections (n D 75 [14.5%]). Forty-nine (9.5%) women reported that they were not aware of the HPV vaccine. Time of HPV-vaccination with regard to sexual debut Overall, 355 (59.7%) participants provided information on time of vaccination (first dose) and age at first intercourse; 186
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Table 2. Responses to attitude and knowledge items among unvaccinated (n D 516) and vaccinated (n D 595) women, Germany 2012—13
I am convinced of the effectiveness of the HPV-vaccine Vaccination against HPV has strong side effects
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I felt sufficiently informed to opt for or against HPV-vaccination Vaccination against HPV replaces the need for cervical cancer screening Since condoms protect sufficiently against infection, HPV vaccination is not necessary
Vaccination status
Strongly agree (%)
Somewhat agree (%)
Slightly agree (%)
Do not agree (%)
Do not know (%)
p-value
unvaccinated vaccinated unvaccinated vaccinated unvaccinated vaccinated unvaccinated vaccinated unvaccinated vaccinated
8.9 32.4 17.1 3.4 20.0 37.7 2.1 1.5 1.6 0.2
31.2 47.6 19.4 8.7 21.1 32.3 4.3 2.3 6.6 1.8
27.7 8.9 9.9 16.5 19.8 17.0 9.1 10.2 17.4 6.9
16.5 2.5 4.1 64.7 29.3 9.9 66.9 76.5 52.5 86.2
16.7 8.6 49.6 6.7 9.0 3.5 17.6 9.4 21.9 4.9
— < 0.01 — < 0.01 — < 0.01 — < 0.01 — < 0.01
(52.4%) received the first dose before sexual debut. This proportion decreased with an increase in age at time of vaccination (Fig. 2). For example at the age of 17 y, more than 60% had already had sexual intercourse.
Discussion Our study demonstrated the feasibility of recruiting young women into health research via a social networking site in Germany. Different targeting strategies optimized the composition of the study population with respect to the proportion of lower educated women and those with a migrant background, groups which are often underrepresented in self-selected samples. Over 90% of participants were aware of HPV. Self-reported HPV vaccination coverage was 53%, and uptake was independently associated with a physician’s recommendation and knowledge of HPV vaccine effectiveness and safety. Previous studies found that social networks are a useful tool to recruit young persons, even when addressing sensitive research questions.14-17 The anonymity guaranteed by online surveys are of benefit if study topics are personal or taboo, such as questions on sexuality as in the case of HPV, where household or schoolbased recruitment strategies may be less favorable.16,17 Recently, a study used Facebook to collect data on knowledge of HPV and cervical cancer among young women in Australia.18 In that study, characteristics of the study population did not differ from data from the National Bureau of Statistics with regard to geographic region, ethnicity and socioeconomic status; however, women aged 16–17 y and those with higher education were underrepresented. Samples recruited from social media networks tend to have an overrepresentation of females and younger adults.15 One study, which compared traditional with online advertisement recruitment found that men, young adults, ethnic minorities, and a high school education or less were more likely to be recruited via online advertizing.19 In the current study, we were able to adjust the targeting strategy based on an interim analysis of key characteristics, thereby optimizing the study sample composition; the focused targeting strategy applied during the second phase was successful in increasing the proportion of lower educated women and women with a migrant background.
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However, despite optimizing the targeting strategy, we observed a loss of potential participants during the click-through process until the start of the questionnaire, and still recruited a higher proportion of women with a higher education status compared with the general German female population. Keeping the advertisement neutral in appearance and text (i.e., health-related advertisements without an obvious link to vaccine-related subjects) may limit selection to those likely to have an interest in HPV vaccination. Overall, Facebook provided an easy means of contact with young women in Germany. The targeting strategies in our study were developed in cooperation with a company specialized in this field. Facebook provides access to online tools to create targeting advertisements, but for those not working in this field, it requires some time to get familiar with these tools. The average perceived likelihood of developing cervical cancer was low at 27% in our population, and was smaller in those with higher educational attainment and who had received the HPV vaccine. One study conducted in Italy prior to the introduction of HPV vaccines found that women who perceived they had a high risk of contracting HPV infection were more likely to receive the vaccine in the future.20 In contrast, in our study, women with a higher perceived risk of being treated for cervical cancer in the future had a lower chance of being vaccinated against HPV, although in multivariate analysis this was not statistically significant (data not shown). A possible explanation is that our study was conducted after introduction of the HPV vaccine in the population. Women who were already been vaccinated against HPV might have had an even higher perceived risk before vaccination (which initiated the decision), and the perceived risk of developing HPV-related disease decreased after receiving the vaccination. Regarding attitude and knowledge items, vaccinated women were more often convinced of the effectiveness of the vaccine and were less often concerned about side effects. Two recently published reviews found that doubts about vaccine effectiveness, concerns of safety, and fear of side effects were among the most common themes related to HPV vaccine uptake.11,21 Knowledge regarding HPV has been shown to be relatively low in various settings,21-23 although it has increased since introduction of HPV vaccines.24 In our study, 76.5% and 66.9% of vaccinated and unvaccinated women knew that HPV vaccination cannot replace
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Table 3. Factors potentially associated with HPV-vaccine uptake among 1,161 females aged 18–25 y, Germany 2012–13
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Variable/Category Age (years) 18–19 20–22 23–25 Region of residency Eastern federal states Western federal states Migrant background No Yes Education Less than university access degree or still in education University access degree Religion Christian Islamic other none HPV-vaccination recommended by physician No Yes Vaccinated against tetanus No Yes Level of being informed about HPV vaccines less well/ poorly informed Very well/well informed Actively sought information on HPV vaccination No Yes Convinced of HPV vaccine effectiveness No1 Yes2 Concerns of HPV vaccine severe side effects No1 Yes2 Feels adequately informed to opt for/against HPV vaccination No1 Yes2 Opinion that HPV-vaccination replaces cervical cancer screening No1 Yes2 Opinion that condoms protect against HPV, thus vaccination is not necessary No1 Yes2
HPV vaccination coverage (%)
Crude OR (95% CI)
Adjusted OR (95% CI)
61.6 62.5 27.5
1 1.0 (0.8–1.4) 0.2 (0.2–0.3)
1 1.2 (0.7–2.1) 0.5 (0.2–1.0)
59.2 51.9
1 0.7 (0.5–1.0)
ns
54.3 51.2
1 0.4 (0.7–1.2)
ns
48.9 55.6
1 1.3 (1.0–1.6)
ns
55.8 57.1 41.2 48.8
1 1.1 (0.6–1.8) 0.6 (0.2–1.5) 0.8 (0.6–1.0)
ns
10.6 78.0
1 29.9 (20.2–44.4)
1 33.3 (15.6–70.7)
18.5 54.9
1 5.4 (2.0–14.2)
ns
35.0 68.4
1 4.0 (3.1–5.2)
ns
37.4 62.9
1 2.8 (2.2–3.6)
ns
15.0 60.5
1 8.7 (4.9–15.3)
1 4.0 (1.5–10.8)
94.0 41.6
1 0.04 (0.03–0.1)
1 0.03 (0.01–0.06)
28.1 62.1
1 4.2 (3.0–5.8)
ns
56.9 51.2
1 0.8 (0.6–1.1)
ns
65.4 28.6
1 0.2 (0.1–0.3)
1 0.2 (0.1–0.4)
95% CI, 95% confidence interval; OR, odds ratio; ns, statistically not significant; 1 “I do not agree”; 2 “I strongly/somewhat/slightly agree.”
regular cervical cancer screening. However, 15% of the entire study population did at least “slightly agree” with that item, revealing the need for educational interventions to improve the level of knowledge about HPV transmission routes and prevention of HPV-related diseases. We found an HPV vaccination coverage of 53%, which is comparable to results (49%) of a telephone survey among 18–20-y-old females conducted in Germany in 2010.10 In agreement with findings of other studies, HPV vaccine uptake was strongly associated with a vaccination recommendation from a physician. Although a study in the Netherlands showed the complexity of the decision-making process as to whether or not to be
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vaccinated against HPV,25 a primary healthcare provider played a crucial role in initiating or completing the vaccine course, at least in settings where structured (e.g., school-based) vaccination programs did not exist.26,27 Only 11% of women in our study who had no doctor’s recommendation received the HPV vaccine compared with 80% of those who were advised to have the vaccination. This highlights the importance of physicians in influencing an individual’s decision-making process to receive the vaccine.28 Positive attitudes of physicians toward the HPV vaccine have been shown to be the main driving force in vaccine uptake, whereas the option was hindered by perceived parental or girls concerns regarding safety and side effects.21,28,29
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Figure 2. Proportion of women vaccinated before (light gray bars) and after (dark gray bars) sexual debut, Germany 2012–13 (n D 355).
In our study, less than 4% of women reported that they were advised against HPV vaccination by a physician. A more detailed analysis regarding specialization or residency of those physicians was not possible since this information was not assessed in the questionnaire. When time of HPV vaccination with regard to sexual debut is interpreted, the age of study participants and endorsement date of the recommendation for HPV vaccination have to be taken into account. Women aged 25 y at the time of our study were 20 y old when HPV vaccination was adopted into the national immunization schedule in Germany. Therefore, it is not surprising that a large proportion of the women received the vaccine after sexual debut and that this proportion increased with increasing age. Results on age of first sexual intercourse in Germany have been previously assessed by a representative survey on youth sexuality in 2009.30 This study revealed that 53% of women with (our study 69%) and 66% without a migrant background (our study 75%) had experienced their first sexual intercourse at the age of 17. Whether these differences could be explained through the anonymity of our survey can only be assumed since comparison of results are limited owing to differences in study populations and study time. Our study benefits from its innovative design and large sample size, including women from different ethnic and socioeconomic backgrounds across the country. We were able to recruit more than 1000 women of the targeted population in less than 4 wk. Optimizing the targeting strategy, we were able to recruit a study population that resembled more closely the general female population in that age group living in Germany. Nevertheless, some limitations of our study need to be acknowledged. First, we used a cross-sectional design that generally precluded determination of causal relationships between outcomes and potentially relevant factors. Second, younger adolescents were not included, although they are the primary target for HPV vaccination. It is possible
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that HPV-related awareness, knowledge and attitude, and HPV vaccine uptake in the younger age group differs from that in our study population. Third, recruiting via a social network itself and the low click-through rate may have introduced selection bias, and thus representativeness of the sample could not be fully determined. Nevertheless, although women with a higher education and younger women were over-represented in our study, several important characteristics of our study sample were comparable to the general female population in Germany. Fourth, information on sexual behavior, vaccination status, and other characteristics was self-reported and could be subject to misclassification. Fifth, it could not be validated whether the stated age and other characteristics of the participant Facebook accounts were correct. Finally, repeated participation in the survey could not be ruled out and might have biased both the demographics of the study population and the results regarding HPV vaccine-related issues. However, providing a valid e-mail address for the lottery draw and excluding participants who completed the questionnaire in a very short time should have reduced this possibility. These limitations have to be borne in mind when the results on HPV vaccine-related knowledge, attitudes and uptake are compared with data using traditional recruitment methods. In conclusion, we were able to show that social media networks can be used as a recruitment tool for health-related online surveys among adolescents and young adults. In addition, study sample composition can be manipulated by applying adjusted or more focused targeting strategies. Given the increasing number of Facebook users in this age group, recruiting via this networking site has the potential to achieve large samples of representative surveys within a short time period. Results on HPV vaccinerelated knowledge, attitudes and uptake were comparable to results of studies using traditional recruitment methods, and indicated a further need for promotion of knowledge of HPVvaccines in terms of benefit and harm among young women. In addition, physicians should be aware of their important role in the decision-making process to opt for or against HPV vaccination when discussing this issue with their young patients.
Methods Advertising on Facebook Use of Facebook requires initial registration using a valid e-mail address. After log-in, the user can adapt her/his profile and add personal data, such as place of residence, gender, age, or personal interests. These data—if not hidden via the privacy settings of Facebook—can be used by third parties for paid targeted advertisements to reach people with interests that are similar to the products offered or products that are gender-specific (https:// www.facebook.com/business/products/ads). These advertisement strategies can be simple, such as targeting a large group of people (e.g., advertisements are displayed to all women living in Germany), or focused, when more specific targeting options are used (e.g., advertisements are displayed to women aged 18–25 y living in Germany, to Turkish-speaking users, to those with an interest in a certain pop star). After implementation, performance of the
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targeting strategy can be monitored using the so-called “ads manager.” This online tool provides data on total views of the advertisement (i.e., number of times it has been shown to a targeted user), the number of clicks on it, the click-through-rate (the number of clicks on an advertisement divided by the number of times it has been viewed), and the conversion rate (the proportion of visitors on the study website who completed the questionnaire). Targeting strategy Inclusion criteria for participation were (1) female gender, (2) age 18–25 y, and (3) resident in Germany. The age group was chosen since these women already had decided for or against HPV vaccination (HPV vaccination in Germany is free of charge only between 12 and 17 y of age). In addition, for legal reasons, females younger than 18 y were not permitted to participate in the lottery draw, vouchers for which were used as an incentive to complete the questionnaire in the current study. Between December 2012 and January 2013, paid advertisements were shown on Facebook to recruit eligible women for an online survey related to HPV immunization in Germany. The targeting strategy was developed in cooperation with a company specialized in online display advertising and landing page optimization. In the first study phase (10–23 December 2012) we applied a simple strategy. The advertisements comprised an image (e.g., showing young women of various ethnic backgrounds, female physicians, or health-related symbols such as a stethoscope) combined with variations of short titles (e.g., “Your participation is needed”) and short text messages (e.g., “Take part in a survey of the Robert Koch Institute”) and were displayed to Facebook users if they identified themselves as female, age 18–25 y, and living in Germany. Some examples of advertisements utilized in this study can be found in the Supplemental Materials. In the second study phase (8–17 January 2013) we applied a focused targeting strategy, which was guided by results of an interim analysis of the first study phase, by adding one additional target set: advertisements were displayed to Facebook users who additionally had certain fashion brands, rap stars, TV series, or TV channels listed on their profile. The interim analysis had indicated that women who were migrants were underrepresented in the first study phase, so we also included a target set of Turkish TV or pop stars and different languages (e.g., Polish, Russian, or Turkish) for relevant migrant groups in Germany to increase the participation rate of this group. However, as with the simple targeting strategy, titles and text messages as well as the questionnaire were provided in the German language only. There were 39 different advertisements (21 in phase one and 18 in phase two) during the study period. By clicking on the advertisements, women were directed to the landing page of the survey website, which provided information on the study aims and background. As an incentive, vouchers for an online lottery draw worth €20 each were promised to participants who gave their email address at the end of the questionnaire. Questionnaire We used a structured questionnaire consisting of 26 questions in the German language to collect information on (1) HPV
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awareness, (2) knowledge, attitude, and behavior related to HPV immunization, as well as (3) sociodemographic factors. At the beginning of the survey, participants were asked to rate their perceived likelihood of ever (1) developing cervical cancer or (2) being treated for cervical precancerous lesions (response scale 0–100%) and whether they “have ever heard of the HPV vaccine” (response options: “Yes,” “No,” “Don’t know”). Women who had heard of the vaccine were then asked how well informed they felt about the vaccine (“very well,” “well, “less well,” “poorly” informed). Their attitude toward and knowledge of HPV vaccines was assessed by providing five-point Likert scale response options (“I strongly agree,” “I somewhat agree,” “I slightly agree,” “I do not agree,” and “I don’t know”) to the following questions: “I am convinced of the effectiveness of the HPV-vaccine,” “Vaccination against HPV has severe side effects,” “I felt sufficiently informed to opt for or against HPV vaccination,” “Vaccination against HPV replaces the need for cervical cancer screening,” and “Since condoms protect sufficiently against infection, HPV-vaccination is not necessary.” In addition, women were asked whether they had actively sought information about vaccinations in general (“Yes,” “No,” “Don’t know”), and if “Yes” how often, and which type of information source (e.g., physician, parents, school, internet, etc.) was consulted most frequently. Regarding receipt of the HPV vaccine, participants were asked whether the vaccine was recommended by a physician and whether they had finally received the vaccine (“Yes,” “No,” “Don’t know”). However, women were not asked where the vaccination took place. Unvaccinated women were in addition asked the reasons for not being vaccinated, with the option of multiple answers. In addition, participants were asked to report if they were vaccinated against tetanus (“Yes,” “No,” “Don’t know”). Finally, sociodemographic data were collected, such as age (years/ month), age at first intercourse (years), immigration status (i.e., at least one parent was an immigrant into Germany), place of residence, level of school education, and religion (Christian, Muslim, other, none). Voxco Survey Software was used for programming and management of the online survey. Data from the questionnaires were self-reported and not validated. Ethical considerations Participation in the study was only possible after agreement to a consent form. The questionnaire was anonymous. Emails for the lottery draw were technically separated from the data of the questionnaire. Women had to be at least 18 y to participate in the study. The study was approved by the German Federal Commissioner for Data Protection and Freedom of Information. Repeated participation Owing to the anonymity of the survey and according to the approval by the German Federal Commissioner for Data Protection and Freedom of Information, the Internet Protocol (IP) address of participants were not saved or tracked. Although women were informed that participation in the study was possible only once, repeated participation could therefore not be ruled out. However, a valid e-mail address was required for the lottery
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draw, and participants who completed the questionnaire in a very short time (defined as 0.8), multiple linear regression was conducted only for linear model 1. To identify independent predictors of HPV vaccine uptake (at least one dose) and completion of the HPV vaccination series, we used univariate analyses for all binary or categorical exposure variables and calculated the crude odds ratios (OR) and 95% confidence intervals (CI). For the purpose of univariate and multivariate logistic regression, data on knowledge were collapsed into two categories “Strongly/somewhat/slightly agree” vs. “I do not agree.” Participants who answered “I do not know” were excluded from the analysis. Variables with a P value < 0.1 in the univariate analysis were included in the initial step for multivariate logistic regression modeling, followed by stepwise backward References 1. Veldhuijzen NJ, Snijders PJ, Reiss P, Meijer CJ, van de Wijgert JH. Factors affecting transmission of mucosal human papillomavirus. Lancet Infect Dis 2010; 10:862–74; PMID:21075056; http://dx.doi.org/ 10.1016/S1473-3099(10)70190-0 2. Schiffman M, Castle PE, Jeronimo J, Rodriguez AC, Wacholder S. Human papillomavirus and cervical cancer. Lancet 2007; 370:890–907; PMID:17826171; http://dx. doi.org/10.1016/S0140-6736(07)61416-0 3. Delere Y, Meyer C, Reiter S. Universal immunisation with human papillomavirus (HPV) vaccine among females aged 12-17 recommended in Germany. Euro Surveill 2007; 12:E070405.2; PMID:17439800 4. Kjaer SK, Breugelmans G, Munk C, Junge J, Watson M, Iftner T. Population-based prevalence, type- and age-specific distribution of HPV in women before introduction of an HPV-vaccination program in Denmark. Int J Cancer 2008; 123:1864–70; PMID:18661520; http://dx.doi. org/10.1002/ijc.23712 5. Iftner T, Eberle S, Iftner A, Holz B, Banik N, Quint W, Straube AN. Prevalence of low-risk and high-risk types of human papillomavirus and other risk factors for HPV infection in Germany within different age groups in women up to 30 years of age: an epidemiological observational study. J Med Virol 2010; 82:1928–39; PMID:20872721; http://dx.doi.org/10.1002/jmv.21910 6. Delere Y, Remschmidt C, Leuschner J, Schuster M, Fesenfeld M, Schneider A, Wichmann O, Kaufmann AM. Human Papillomavirus prevalence and probable first effects of vaccination in 20 to 25 year-old women in Germany: a population-based cross-sectional study via home-based self-sampling. BMC Infect Dis 2014; 14:87; PMID:24552260; http://dx.doi.org/10.1186/ 1471-2334-14-87 7. Lehtinen M, Paavonen J, Wheeler CM, Jaisamrarn U, Garland SM, Castellsague X, Skinner SR, Apter D,
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removal of all variables with a P value > 0.05 to obtain the final model. Two-sided hypothesis tests were performed, and a P value < 0.05 was considered statistically significant. Missing data were treated as such and not imputed. The statistical software package STATAÒ , version 11 (STATA Corp.) was used. Disclosure of Potential Conflicts of Interest
No potential conflicts of interest were disclosed. Acknowledgments
We would like to thank all the women who participated in the study. Funding
The study was funded by internal funds of the Robert Koch Institute. Contributions
All authors were involved in the conception and design of the study. C.R. performed the data analysis and drafted the article. All authors contributed to data interpretation and the final version of the manuscript. Supplemental Materials
Supplemental materials may be found here: landesbioscience.com/journals/vaccines/article/29541/
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