HPV vaccination coverage among women aged 18–20 years in Germany three years after recommendation of HPV vaccination for adolescent girls

Abstract

Objective: Routine immunization of adolescent girls aged 12–17 y against human papillomavirus (HPV) was recommended in Germany in March 2007. We aimed to assess HPV-vaccine uptake and knowledge about post-vaccination cervical cancer screening and condom use in women aged 18–20 years, three years after adoption of HPV-vaccination into the routine vaccination schedule.

Results: Overall 2,001 females participated in our study. Of these, 49% reported receipt of a complete three-dose course of HPV-vaccines; 11% received 1 or 2 doses. Living in East Germany, high educational status, and interest in health-related issues were independently associated with HPV-vaccination. Misconceptions among survey-participants were rare: Only 8% believed that HPV-vaccination would obviate the need for cervical screening and 1% that condom use would be dispensible after vaccination.

Methods: In 2010, a nationwide cross-sectional telephone-survey was performed among randomly-selected women aged 18–20 years living in Germany. Telephone interviews were conducted by a large professional market research institute as part of a daily omnibus survey.

Conclusion: HPV-vaccination coverage is low in Germany. The results indicate that there is an urgent need for the implementation of a coordinated adolescent vaccination program to facilitate access to vaccination, including balanced information tailored to this age group. Otherwise, the HPV-vaccination effort will fall short of reaching its maximum public health benefit.

Keywords: :

• HPV
• vaccine uptake
• cross-sectional survey
• telephone interview
• Germany

Introduction

Anogenital infections with human papillomavirus (HPV) are predominantly sexually transmitted and the majority of (>50%) sexually active women will be infected by one or more genital HPV types at some point in time.¹ Most HPV infections are transient, but persistent infections can progress over many years to cervical precancer and cancer. Nearly 5,000 incident cervical cancer cases are diagnosed annually in Germany and approximately 70% of cases are associated with HPV genotypes 16 and 18.²

Two vaccines against HPV are available on the market, and HPV vaccination was adopted into the German routine immunization schedule for 12- to 17-y-old girls in March 2007.³ A complete course of HPV vaccination (consisting of three vaccine doses) is free of charge in this target age-group.

Since in Germany vaccination coverage is routinely assessed only at school entry at the age of 5–7 y, HPV vaccination coverage in adolescents at the country-level is unknown. We conducted a cross-sectional survey three years after initiation of routine HPV immunization to assess (1) HPV vaccine uptake among women aged 18–20 y at the country-level and (2) knowledge on post-vaccination cervical cancer screening and condom use in this age-group.

Results

Of 3,048 initially contacted women, 2,001 (65.6%) participated in this study. Characteristics of the study sample are presented in Table 1.

Table 1. Characteristics of the study sample and the general female population aged 18–20 y living in Germany

	Study sample		General female population aged 20 y* (Germany)
	n (unweighted)	% (95% CI)^†	n	%
Total	2,001	100	476,721	100
Residency
WFS	1,769	81.6 (79.5–83.6)	378,816	79.5
EFS	232	18.4 (16.4–20.5)	97,905	20.5
Educational Status
low	155	7.7 (6.6–9.0)	82,000	14.7
medium	481	24.0 (22.1–25.9)	157,000	33.6
high	1,348	68.3 (66.2–70.3)	195,000	41.8
education not yet completed	-	-	31,000	6.6
not reported	-	-	11,000	3.3
Receipt of ≥ 3 doses of HPV vaccine
yes	963	48.5 (46.3–50.8)	unknown
no	1,021	51.5 (49.2–53.7)	unknown
Receipt of at least 1 dose of HPV vaccine
yes	1,203	60.2 (58.0–62.4)	unknown
no	794	39.8 (37.6–42.0)	unknown
Belief that condom use is dispensable after HPV vaccination
yes	27	1.3 (0.9–1.9)	unknown
no	1,966	98.7 (98.1–99.1)	unknown
Belief that HPV vaccination obviates participation in cervical cancer screening
yes	155	7.8 (6.7–9.1)	unknown
no	1,815	92.2 (90.9–93.3)	unknown
How often do you concern yourself with health-related issues?
seldom/never	758	37.4 (35.2–39.6)	unknown
very often/often	1,243	62.6 (60.4–64.8)	unknown

* Data by the German federal statistical office (www.genesis.destatis.de); ^†Weighted data; EFS, Eastern federal states; WFS, Western federal states.

Among women who reported their HPV vaccination status (99.8% of respondents), 60.2% (95% CI: 58.0–62.4) had received at least one HPV vaccine dose and 48.5% (95% CI: 46.3–50.8) a complete three-dose course. Of the vaccinated women, 67% did not know the name of the HPV vaccine product they had received.

In univariate analysis, females living in former East German Federal States (EFS) were significantly more likely to be vaccinated than females living in former West German Federal States (WFS) (69% vs. 58%; p < 0.001). Moreover, women with a high educational status had a significantly higher vaccination coverage compared with those with a low educational status (62% vs. 50%; p = 0.007). In multivariate analysis, living in an EFS, high educational status, and interest in health-related issues were independently associated with higher uptake of HPV vaccines (Table 2).

Table 2. Factors associated with HPV vaccine uptake and misconceptions related to condom use and cervical cancer screening

		Odds Ratio*
	Proportion in % (95% CI)*	Univariate	Multivariable
Outcome: Receipt of HPV vaccines^a
Residency
WFS	58.3 (55.9–60.5)	1 (ref)	1 (ref)
EFS	69.1 (62.8–74.7)	1.60 (1.26–2.04)^††	1.55 (1.21–1.97)^††
Educational status
low	50.5 (42.5–58.5)	1 (ref)	1 (ref)
medium	59.2 (54.7–63.6)	1.43 (0.99–2.06)	1.39 (0.96–2.01)
high	61.9 (59.2–64.5)	1.59 (1.14–2.23)^†	1.54 (1.10–2.16)^†
How often do you concern yourself with health-related issues?
seldom/never	56.8 (53.2–60.4)	1 (ref)	1 (ref)
very often/often	62.3 (59.5–65.0)	1.25 (1.04–1.51)^†	1.23 (1.02–1.48)^†
Outcome: Belief that condom use is dispensable after HPV vaccination
Residency
WFS	1.5 (1.0–2.1)	1 (ref)	n.s.
EFS	0.4 (0.1–3.0)	0.29 (0.06–1.47)
Educational status
low	4.1 (2.0–8.4)	1 (ref)	1 (ref)
medium	2.3 (1.3–4.2)	0.55 (0.20–1.50)	0.55 (0.20–1.50)
high	0.4 (0.2–0.9)	0.09 (0.03–0.30)^††	0.09 (0.03–0.30)^††
HPV vaccination^a
yes	0.8 (0.4–1.4)	1 (ref)	n.s.
no	2.0 (1.3–3.3)	2.73 (1.21–6.18)^†
How often do you concern yourself with health-related issues?
seldom/never	1.8 (1.1–3.0)	1 (ref)	n.s.
very often/often	0.9 (0.5–1.7	0.51 (0.23–1.12)
Outcome: Belief that HPV vaccination obviates participation in cervical cancer screening
Residency
WFS	8.1 (6.9–9.4)	1 (ref)	n.s.
EFS	6.7 (4.1–10.9)	0.82 (0.53–1.29)
Educational status
low	34.1 (26.6–42.5	1 (ref)	1 (ref)
medium	9.4 (7.0–12.4)	0.20 (0.13–0.32)^††	0.22 (0.14–0.36)^††
high	4.3 (3.3–5.5)	0.09 (0.06–0.13)^††	0.09 (0.06–0.14)^††
HPV vaccination^a
yes	6.1 (4.8–7.7)	1 (ref)	1 (ref)
no	10.3 (8.4–12.7)	1.78 (1.28–2.47)^††	1.60 (1.12–2.27)^†
How often do you concern yourself with health-related issues?
seldom/never	11.9 (9.7–14.6)	1 (ref	1 (ref)
very often/often	5.4 (4.2–6.8)	0.42 (0.30–0.59)^††	0.45 (0.32–0.65)^††

* Weighted data; ^†p ≤ 0.05; ^††p ≤ 0.001; ^adefined as having received at least one dose of HPV vaccine; CI, confidence interval; EFS, Eastern federal states; ns, non-significant; ref, reference category; WFS, Western federal states.

Of all respondents, 8% believed that HPV vaccination would obviate the need for participation in cervical cancer screening. This misconception was significantly more common in unvaccinated than vaccinated females (10% vs. 6%; p = 0.001). Among women with the lowest educational status, 34% believed that HPV vaccination would make participation in regular screening unnecessary compared with 9% of women with a medium and 4% of women with the highest educational status (for both: p < 0.001). Significant differences in knowledge between women living in the EFS or WFS were not found (Table 2).

Only 1% of 18- to 20-y-old women believed that condom use would be dispensable after HPV-vaccination (Table 1). Similar to the results found for cancer screening, this proportion was significantly higher in unvaccinated compared with vaccinated women (2.0% vs. 0.8%; p = 0.016) and in females with low educational status compared with females with a high educational status (4.1% vs. 0.4%; p < 0.001). There were no significant differences between women from EFS and WFS (Table 2).

In multivariate analysis, only low educational status was associated with the misconception that condom use would be dispensable after HPV vaccination. In contrast, low educational status, not being vaccinated against HPV, and never/seldom being concerned about health-related issues were factors independently associated with the misconception that HPV vaccination would obviate the need for participation in cervical cancer screening (Table 2).

Discussion

After adoption of HPV-vaccination into the national immunization schedule in 2007, vaccination coverage in the 3 oldest eligible age-cohorts remained low. In the absence of an immunization registry, these are the first countrywide HPV vaccination coverage data for Germany. The study is also the first to provide empirical data suggesting that HPV vaccination did not promote misconceptions related to sexual behavior or cervical screening in Germany. Such data, including information on subgroups with lower vaccine uptake and misconceptions, are urgently needed to develop tailored communication strategies.⁴

Our coverage estimates are in line with two local, school-based surveys in Germany. In the federal state of Brandenburg, HPV vaccination coverage among approximately 4,000 girls attending 10th grade school in 2012 was 39.5%.⁵ In Berlin, 41% of 10th grade female students who presented their vaccination cards had received three HPV vaccine doses.⁶

Reasons for the limited uptake of HPV vaccines in Germany seem to be complex. Since their introduction into the national immunization schedule by the German Standing Committee on Vaccination (STIKO), effectiveness and safety of HPV vaccines were controversially discussed in the media. Two deaths in young females falsely attributed to the vaccination and a publication of 13 public health experts criticizing the STIKO recommendation in Germany may have contributed to uncertainty among young women and their parents.⁷ While public criticism and vaccine safety concerns may be driving factors for a lower acceptance,⁸ surveys have shown that a physician’s recommendation has the highest impact on the decision-making process for or against vaccination both in the US^9-12 and in Germany.¹³ Physicians have the opportunity to dispel misconceptions or safety concerns. It can be assumed that public criticism has also led to uncertainties among providers,^14,15 but data on knowledge, attitude and practices related to HPV vaccination within this group are unavailable in Germany.

Misconceptions on screening participation and condom use post-vaccination were rare in our survey. Most participating women were aware that HPV vaccination would not obviate the need for cervical screening. These findings are in keeping with results from a study in France. Knowledge on cervical cancer prevention was better among females aged 21–23 y who had been vaccinated against HPV than among those who had not (60.0% vs. 25.6%, p = 0.06).¹⁶ However, one third of women included in our survey with a low educational status believed that HPV vaccination would make cervical cancer screening unnecessary. The majority of our respondents knew that condom use was important even after HPV-vaccination. Concerns about a change in sexual behavior (e.g., less condom use) in vaccinated adolescents and adults are often expressed, but seem to be marginal. According to a recently published U.S. study, girls who had been vaccinated against HPV were not more likely to acquire sexually-transmitted infections or to become pregnant.¹⁷ In the previously mentioned French study, >85% of participants who were sexually active used condoms, irrespective of HPV vaccination status.¹⁶

In our study, a higher educational status and general interest in health-related issues were significantly associated with HPV vaccine uptake and better knowledge of HPV vaccination. Moreover, acceptance of HPV vaccination was significantly higher in the EFS; a phenomenon that is already known from other vaccinations. Reasons for higher acceptability in the EFS are complex and not yet adequately investigated. One reason may be that—although reunification of East and West Germany took place over 20 y ago—mandatory vaccination practices in the former German Democratic Republic still influence today's general attitude and behavior toward vaccinations.^18-20 Furthermore, differences in vaccination policies at the federal state level can be observed between the Eastern and Western states.

Finally, reaching 12- to 17-y-old adolescents is in particular difficult in Germany, especially since there are no school-based immunization programs or other alternative approaches such as vaccine reminder via short text messages (sms) or via invitation letters in place. In addition, a concerted communication strategy for HPV vaccination is lacking in Germany.

Low uptake is likewise seen in other countries without national school-based immunization programmes. In Paris, France, only 20% of 14- to 23-y-old females were vaccinated against HPV in 2009.²¹ Data from the National Health Insurance Information System in France indicated an HPV vaccination uptake of nearly 30% for three doses among 14-y-old girls.²² France and Germany have comparable vaccination delivery strategies. An adolescent or one parent has to make a doctor’s appointment to get vaccinated. In most cases she needs written informed consent from her parents or one parent must accompany her. This could be considered a high barrier to vaccination. In contrast, school vaccination programs can provide adolescents easy access to HPV vaccination. In England, more than 80% of girls aged 12–13 y completed a three-dose HPV-vaccine course in 2010/11 through a school-based program.²³

Our study results are subject to some limitations. Participants consisted of all women in the daily omnibus survey who agreed to be re-interviewed. This could have led to selection bias. However, the selection may not be strong in regards to the study topic because the omnibus survey is a multi-topic study design. Second, only 7.7% of study participants had a low and 68.3% a high educational status compared with 14.7% and 41.8% of 20-y-old females among the general population in Germany.²⁴ Since higher education was associated with higher vaccine uptake, the true HPV vaccination coverage is likely to be even lower than estimated in our study. Third, HPV vaccination status was self-reported. This might have led to potential under- or over-reporting. However, since HPV-vaccines became available only three years prior to the conduct of this survey and were intensively discussed in the media, and since three doses are required, we believe that recall problems are unlikely to have played a major role in our survey. Fourth, women were interviewed in German only, so our sample only represents the German-speaking young female population and is therefore unable to identify potential challenges in the population with a migratory background. Fifth, we focused on demographic, educational and knowledge factors potentially influencing HPV vaccine uptake. System-based factors (e.g., place of delivery) were not assessed as reasons for non-vaccination, but might play a crucial role. Finally, only women with a landline number were included in our study. It is not known whether the exclusive use of mobile phones might be associated with different knowledge on and uptake of HPV-vaccines in this age-group.

Conclusion

Our survey provides important population-based data on HPV vaccine uptake and preventive behavior in Germany. Since our survey covered only the eldest three birth-cohorts eligible for free HPV-vaccination, and since it takes time for recommendations to be implemented, this survey should be repeated to monitor potential trends in HPV vaccine uptake. The results indicate that there is an urgent need for the implementation of a coordinated program for adolescents to facilitate easy access to vaccination, including balanced information tailored to this age group, particularly for less educated population subgroups. Otherwise, the HPV vaccination effort will fall short of reaching its maximum public health benefit.

Materials and Methods

Between the 19th of July and the 4th of August in 2010, a cross-sectional telephone-survey was performed among females aged 18–20 y in Germany. In Germany, only girls aged 12–17 y are eligible for HPV vaccination free of charge (with few exceptions, depending on the respective health insurance company). Hence, we focused on the age-group 18–20 y, since these birth cohorts had had the opportunity to receive a 3-dose-course of HPV vaccines from 2007 onwards, but were too old in 2010 to be eligible for starting a complete HPV vaccines series free of charge (this permitted an assessment of the receipt of incomplete vaccination series). Computer-assisted telephone interviews (CATI) were conducted by a large professional market research institute (forsa: Gesellschaft für Sozialforschung und statistische Analysen) in a subsample of participants within a daily omnibus survey. Forsa's omnibus survey in Germany targets all German speaking individuals, aged 14 y and older, living in private households equipped with a telephone. Female participants of the omnibus survey aged 18–20 y were contacted to be included in this HPV survey. A 5-item HPV-specific questionnaire in addition to standardized questions of the omnibus survey (that include demographic data, information on how frequently the interviewee concerns him/herself with health-related issues) was applied to collect the following data:

• Data on HPV-vaccination (i.e., receipt of HPV vaccine, number of doses, name of product)

• Knowledge of HPV vaccination and cervical cancer screening participation

• Knowledge of HPV vaccination and condom use

The German school system is hierarchically tiered. Basic primary school (grades 1–4) is followed by the secondary general school that covers grades 5 to 9 (low educational status) or 5 to 10 (medium educational status). Secondary schools (“Gymnasium”), which cover grades 5–13 and qualify for university studies, were defined as “high status education.” Calculations of vaccination coverage and prevalence of specific population characteristics were weighted for geographic region and age. Unless otherwise indicated, the data presented in this paper are weighted data. Data analysis was performed using the software package PASW 18.0 (SPSS Inc.). Proportions were calculated by using procedures for the analysis of complex samples. In our study a p-value < 0.05 was considered to indicate a statistically significant difference. Odds ratios (OR) and 95%-confidence intervals (CI) were calculated as appropriate. Univariate and multivariable logistic regression analyses were performed to identify factors associated with HPV vaccine uptake or beliefs.

Abbreviations:
HPV	=	human papillomavirus
STIKO	=	German Standing Committee on Vaccination
CATI	=	computer-assisted telephone interview
CI	=	confidence interval

Disclosure of Potential Conflicts of Interest

The authors declare no conflict of interests. The study was exclusively financed by RKI.