Knowledge of human papillomavirus among high school students can be increased by an educational intervention

Abstract

The aim of this study was to evaluate the effect of an educational intervention concerning human papillomavirus (HPV) directed at Swedish first year high school students. The intervention consisted of a class room lesson, a website and a folder. Outcome variables were knowledge of HPV and attitudes to preventive methods such as HPV vaccination, condom use and Pap smear testing. An intervention group (n = 92) was matched with two comparison groups (n = 184). At baseline, the median score for HPV knowledge was one out of 10 in both groups. At follow-up, the median knowledge score had increased to six in the intervention group, but was still one in the comparison group (P < 0.001). Attitudes to HPV vaccination, condom use and Pap smear testing remained the same (P > 0.05). In conclusion, a short school-based intervention can greatly increase the students' knowledge about HPV, but attitudes and behaviours are less easy to influence.

Keywords

HPV prevention vaccination condoms

INTRODUCTION

The incidence of sexually transmitted infections (STIs) has increased in recent years in Sweden, as in the rest of the western world.^1–3 One of the most common STIs is human papillomavirus (HPV) and some HPV types have been associated with development of cervical cancer, as well as other anogenital and oropharyngeal cancers/precancers, and genital warts.⁴ Awareness about the link between an HPV infection and cervical cancer varies, but it is generally low among both adolescents and adults. Consequently, awareness about methods for preventing HPV and cervical cancer is low.^5–11 A Swedish study from 2007 showed that only 1% of the high school students in the study were aware of the association between HPV and cervical cancer and 1% were aware of any vaccine against HPV.⁸ In an Italian study, 30% of the adolescents in the study had heard about HPV infection. As many as 42% of them believed that vaccination was a preventive measure for cervical cancer, 35% believed that condom use was a preventive measure and 36% believed that oral contraception could prevent cervical cancer.⁷

The quadrivalent HPV vaccine has been available in Europe since 2006 and the bivalent vaccine since 2007. The National Board of Health and Welfare in Sweden has recommended a school-based vaccination programme for girls between age 10 and 12 years starting in 2010. The bivalent vaccine was chosen for the school-based programme. However, this decision was contested by the manufacturer of the quadrivalent vaccine and an appeal has been filed. The final decision regarding which vaccine to use in the programme has therefore not been made. At present, the quadrivalent vaccine dominates the sales in Sweden with 95% of the market share.

Another method to prevent the transmission of HPV is the use of condoms. It reduces the risk of transmission by 70% if the male partner consistently uses a condom during all episodes of intercourse.¹² However, this method is problematic regarding compliance. Oral contraceptives have been associated with non-condom use for both men and women (P < 0.05).¹³ Likewise, it has been shown that the intent to use condoms could decline in cases of HPV immunization.¹⁴

Review articles on the efficacy of preventive STI/human immunodeficiency virus (HIV) interventions among adolescents have highlighted the importance of targeting the behaviours that are most amenable to change, e.g. by emphasizing condom skills, frequency of condom use and partner communication techniques.^15,16 Adolescents are not a homogeneous population and interventions should be tailored specifically for subgroups to have optimal effects.¹⁶

Internet-based interventions have shown positive effects on diet and activity outcomes,¹⁷ but the Internet has also been used for HIV prevention. In a randomized controlled trial, it was concluded that Internet-based interventions for adolescents need to be repeated since a single session promoting condoms had only a minor effect on norms regarding condom use.¹⁸

To our knowledge, no intervention aimed at increasing the knowledge of HPV among adolescents has been reported. The principal aim of this study was therefore to evaluate the effect of an educational intervention about HPV and preventive methods for cervical cancer, such as vaccination, condom use and Pap smear testing. Outcome measures were knowledge of HPV and attitudes to preventive methods.

METHODS

Design

A quasi-experimental intervention study.

Population and sample

A strategic sample of first year students from both vocational and theoretical high school programmes were chosen for this study. The vocational high school programmes prepare for handcraft professions and the theoretical programmes prepare for university studies. Four classes from three different high schools were assigned to the intervention group (IG) and nine classes from three other high schools were assigned to two comparison groups (CG1, CG2). The second comparison group was included to check for any bias induced by filling in the baseline questionnaire. The students of comparison group 2 (CG2) did not participate in the study until they completed the follow-up questionnaire. CG2 consisted of students from theoretical study programmes. In the analyses aimed to compare CG1 and CG2, only students in theoretical study programmes were included. CG1 consisted of 36 girls and 15 boys from theoretical programmes. The number of students in each group completing the questionnaires and participating in the intervention is shown in Figure 1.

Figure 1

Number of students in the intervention group ((IG) and the comparison groups (CG1 and CG2) completing the baseline questionnaire, participating in the intervention, and completing the follow-up questionnaire

In each of the three groups, the IG and the two comparison groups, at least 110 students were considered to be required to be able to show a 5% difference between the IG and each comparison group with a power of 80%. The significance level was P < 0.05.

Theoretical framework

The intervention was based on the Health Belief Model (HBM), which is a commonly used model in health campaigns. According to the HBM, people will take action to prevent an ill-health condition if they consider themselves to be susceptible to that condition (perceived susceptibility to a health threat); if they believe it would have potentially serious consequences (perceived severity); if they believe that a course of action available to them would be beneficial in reducing either their susceptibility to or the severity of the condition; and if they believe that the anticipated barriers to, or cost of, taking the action are outweighed by its benefits (perception of the benefits of, costs of and barriers to an action).¹⁹ The intervention was focused on information and discussions regarding perceived susceptibility and perceived severity of the viral infection. The intervention was theory-based, as it has been suggested that theory-based interventions have a more positive effect than those that are not theory-based,^15,20 and included skill training as it has been indicated that this can affect change in sexual behaviour.²¹

Intervention

An intervention took place during the spring of 2009 and involved a one-hour lesson about HPV and preventive methods, with special focus on vaccination and condom use. The lesson started with a 15- to 20-minute long presentation about HPV, its frequency, what it can lead to and how to prevent it. Information on the effectiveness, price and side-effects of the vaccines was included as well as the fact that the vaccines do not protect against all HPV types that can cause cervical cancer and the importance of cervical screening. This was followed by information on how to use a condom and how to put it on. Different types of condoms were introduced and demonstrated. The lesson also included training of practical skills through a game called ‘condom relay race’ (i.e. opening a condom package and practicing rolling it out). The lesson ended with a discussion on STI and HPV prevention and then the students received a specially designed folder about HPV and its prevention, with an enclosed condom. The students were also invited to see the project's website about HPV and other STIs. On the website the students could fill in a quiz about HPV, and the first 10 who answered the questions correctly received a movie theater ticket. A new quiz was available after two weeks and the first 10 who filled it in correctly also received a movie theater ticket.

High school students studying information technology designed the website and the folder. The lesson was held by the first author (registered nurse) together with a specially trained university student.

We hypothesized that the intervention would improve the students' knowledge about HPV and that it would make their attitudes to preventive methods for cervical cancer more positive.

Procedure

Principals of six high schools were contacted and gave their permission for the study.

Before administration of the questionnaires, the students received verbal and written information about the study. Participation was voluntary. At baseline, a brief information text about HPV was available for the students after they had filled in the questions on knowledge, and before they were to fill in the questions regarding attitudes. At follow-up, no information about HPV was included in the questionnaire. After the students had completed the questionnaires, they put them in envelopes and handed them to the researcher or the research assistant. Assent was obtained by completion of the questionnaires or participation in the lesson.

Instrument

To achieve high validity, the questionnaires were designed on the basis of findings in previous studies and most questions had been used previously.^8,22 The baseline questionnaire consisted of 44 questions. Twelve of these questions concerned sociodemographic and sexual health characteristics of the students, four questions concerned general knowledge of STIs and sources of information, and 13 questions concerned HPV knowledge and sources of information. The last 15 questions sought to determine the students' attitudes to HPV vaccines, their attitudes to condom use, alone or in combination with HPV vaccination or contraceptive pills, and the girls' attitudes to Pap smear tests. A few questions were ‘open-ended’ or ‘multiple choice’, but most questions could be answered with ‘yes’, ‘no’ or ‘don't know’. Attitudes regarding condom use and Pap smear in association with vaccination were assessed by means of a 100 mm Visual Analogue Scale (VAS) ranging from ‘completely unlikely’ (0) to ‘highly likely’ (100).

Twenty-three questions from the baseline questionnaire were included in the questionnaire at follow-up. All questions concerning HPV knowledge, four questions concerning attitudes to cervical cancer prevention and the most relevant questions concerning sociodemographic characteristics, sexual health characteristics, and general knowledge of STIs and sources of information, were included. Only the most relevant questions of the baseline questionnaire were included to make the follow-up questionnaire shorter. In the follow-up questionnaire completed by the IG, 11 questions regarding the students' opinions about the intervention were added. The primary outcome variable was knowledge of HPV. Secondary outcome variables were attitudes to cervical cancer prevention such as condom use, HPV vaccination and girls' attitude to attending Pap smear screening in the future. The instrument was tested in a pilot study on 12 high school students. Adjustments to the questionnaire were made on the basis of the opinions expressed by these students.

Data analysis

Data were entered and analysed using the Statistical Package of the Social Sciences (SPSS for Windows v. 16.0). The answers to the 10 questions concerning specific HPV knowledge were divided into two categories, correct answer = 1 and incorrect answer/don't know = 0. To form an index of knowledge, the 10 answers were summed and could add up to a maximum of 10 points if all answers were correct. Differences between the groups were tested for significance at baseline and at follow-up.

Mixed-effects models with a random intercept term for each cluster (classes) and group as a fixed effect were estimated for each ‘question’. Intention to attend for Pap smear if vaccinated was analysed by a linear mixed-effect model. Binary outcome variables were analysed by a logistic mixed-effect model. The knowledge index and influence of HPV vaccination on condom use were markedly non-normally distributed and were therefore dichotomized and analysed as binary variables. The knowledge index was categorized as ‘five or more correct answers’ or ‘less than five correct answers’ and VAS as ‘highly likely’ (90–100 mm) or ‘not highly likely’ (0–89 mm). Correlation between ordinal scaled variables was tested with Spearman's rank-order correlation. Differences were considered significant if P < 0.05. Calculations of the reported percentages were based on the number of students answering each question, and the internal dropout varied between 0% and 5%.

The study was approved by the Regional Ethics Committee in Uppsala, Sweden.

RESULTS

Characteristics

The mean age of the students was 16 years. A majority (76%) were of Swedish origin. Almost half of the students (46%, n = 98) had had sexual intercourse and 67% (n = 66) of them had used a condom at their first intercourse. Twenty-one percent (n = 21) had not used any contraceptive method at their first sexual intercourse. At baseline, the IG had an equal gender distribution (56 girls/58 boys), but the comparison group (CG1) included more girls (n = 78) than boys (n = 43) (P = 0.018). At follow-up, the gender distribution was similar to at baseline. The second comparison group (CG2) had an equal gender distribution.

At baseline, more students in the IG (n = 17) than in the CG1 (n = 6) had tested for an STI (P < 0.001). There was no difference in this respect at follow-up (P = 0.055).

Knowledge of HPV

In an open-ended question about which STIs the students were aware of, only one student at baseline mentioned HPV. At follow-up, 70% (n = 61) in the IG and 7% (n = 7) in CG1 included HPV in the answer (P < 0.001). At baseline, only one student believed HPV to be the most common STI in Sweden, but at follow-up, 30% (n = 25) of the IG and 1% (n = 1) of the CG1 believed so.

As shown in Table 1, the knowledge of HPV in the IG increased significantly after the intervention. Among the students who had heard about HPV at follow-up, students in the IG reported that they had received their information about HPV mainly from school (76%, n = 70), whereas a majority of the students in CG1 reported the media to be the main source of this information (63%, n = 24).

Table 1

Awareness of human papillomavirus (HPV)/HPV vaccine and correct answers to specific knowledge questions about HPV among the intervention (IG) and comparison groups (CG1, CG2)^†

	IGbaseline (n = 114)/follow up (n = 92) (%)	CG1baseline (n = 121)/follow up (n = 110)(%)	CG2follow up (n = 74)(%)	Difference IG versus CG1 at baseline P value*	Difference IG versus CG1 at follow up P value*	Difference CG2 versus CG1 at follow up P value*
Heard of HPV	11/100	12/35	24	0.670	<0.001**	0.017**
Aware of vaccine against HPV	4/64	4/26	6	0.960	0.032**	0.012**
Is HPV a virus that spreads through sex? (yes)	9/92	8/36	23	0.979	0.002**	0.198
Can HPV affect women? (yes)	11/92	11/39	19	0.782	0.003**	0.215
Can HPV affect men? (yes)	4/83	4/11	11	0.768	<0.001**	0.350
Can HPV cause chlamydia? (no)	3/13	2/6	3	0.998	0.153	0.181
Can HPV cause condyloma? (yes)	6/66	3/6	4	0.491	<0.001**	0.653
Do you always notice an HPV infection? (no)	9/74	7/20	18	0.768	0.002**	0.173
Does HPV cause cervical cancer in women? (yes)	10/71	9/33	22	0.940	0.024**	0.192
Does HPV cause other types of cancer? (yes)	0/35	4/4	7	0.640	0.005**	0.659
Can HPV cause herpes infection? (no)	0/15	1/1	1	0.794	0.026**	0.734
How effective is the vaccine? (70%)	48/44	49/50	44	0.548	0.490	0.453
Median number of correct responses on 10 questions concerning HPV knowledge	1/6	1/1	1	0.620	<0.001**	0.912

*P value from a mixed-effects logistic model with a random intercept term for each cluster (class)

^†CG1 completed the baseline and the follow-up questionnaires. CG2 only completed the follow-up questionnaire

**P < 0.05

The median score for HPV knowledge was 1 out of 10 in both groups at baseline (P = 0.620). At follow-up, the median knowledge score was higher in IG than in CG1 (P < 0.001). In IG the median knowledge score had increased to 6, and over 80% of the students had five or more correct answers. In CG1 the median was still 1 and 13% had five or more correct answers.

Attitudes to HPV vaccination, condom use and Pap smear

At baseline, 19 students (15%) in IG and nine students (7%) in CG1 intended to be vaccinated (P = 0.163). Three of these students were boys (2 in IG, 1 in CG1). Three girls in IG (3%) and five girls in CG1 (4%) had been vaccinated against HPV at baseline (P = 0.703). At follow-up, 15 girls in IG (16%) and 15 girls in CG1 (14%) had received the vaccination (P = 0.667). At that time, seven students (8%, 4 girls and 3 boys) in IG intended to become vaccinated and 11 students (11%, 8 girls and 3 boys) in CG1 had this intention (P = 0.344). Attitudes to condom use were equally positive before and after the intervention in both groups. Likewise, attitudes to Pap smear testing did not change in any of the groups after the intervention.

Attitudes to the intervention

More than half of the boys (55%, n = 23) and one-fourth of the girls (25%, n = 12) considered that the intervention had increased their knowledge a lot. A few students, 12% (n = 5) of the boys and 8% (n = 4) of the girls considered that it had not increased their knowledge at all or very little. There was a fair correlation between believing that the intervention had increased the knowledge and a higher knowledge score (r _s = 0.410, P < 0.001). The lesson was seen as the most valuable part of the intervention (55%, n = 51). Almost half of the students (46%, n = 41) had read the folder and 33% (n = 30) had visited the website.

Differences between the two comparison groups at follow-up

Students in CG1 were aware of HPV and HPV vaccines to a higher extent than students in CG2, but no differences were found regarding the specific knowledge questions (see Table 1). Thirteen girls (36%) in CG1 and four girls (11%) in CG2 had been vaccinated against HPV (P < 0.001). No differences were found between the two comparison groups concerning attitudes to condom use and attitudes to Pap smear screening in the event of HPV vaccination.

DISCUSSION

In this study we evaluated the effect of an educational intervention regarding HPV that was developed specifically for adolescents in a school setting. Apart from increased knowledge this intervention did not convincingly show any influence on attitudes to condom use, HPV vaccination and, among girls, the attitudes to Pap smear screening. About 15% of the girls, both in IG and in CG1, were vaccinated between baseline and follow-up, possibly explaining that fewer students at follow-up than at baseline intended to get vaccinated. Filling in the questionnaire might have been enough for some girls to take the steps to vaccination (i.e. the Hawthorne effect), but there was also an intensive direct-to-consumer campaign during this period from one of the vaccine manufacturers. In concordance with previous findings,^7,8 the baseline knowledge was low in this study. At follow-up, the knowledge of HPV was higher in IG than in CG1. The knowledge of HPV was slightly higher in CG1 than in CG2. An explanation for this might have been that the CG1 had gained knowledge through participation in the study.

The attitudes to condom use were equally positive and unaffected by the intervention, regardless of study group. The attitudes to HPV vaccination and Pap smear screening were also unaffected by the intervention. It might be difficult for high school girls to have an attitude about Pap smear screening, since in Sweden women are recommended to attend screening every third year starting from the age of 23 to 25 years.

Despite the availability of an easily read folder and a website designed by peers, the lesson about HPV was the most appreciated part of the intervention. Few of the students reported that they had visited the website, although most adolescents in Sweden have access to the Internet and are frequent computer users.²³ An hour long lesson can apparently make a bigger impression on adolescents than distributed written material. However, written material has also been found to be effective. An educational protocol about HPV and Pap smear tests for adolescents has been reported to increase knowledge of HPV among study participants visiting an adolescent clinic.²⁴ This suggests that simple interventions with limited resources can improve knowledge of HPV. However, knowledge represents only one step in prevention of HPV and cervical cancer. Changing to a preventive behaviour is complex even when good knowledge is obtained; the potential benefits of the preventive behaviour have to be considered to outweigh the cost or other possible barriers.¹⁹

Providing correct, gender-sensitive and balanced information about sexual health issues is a challenging task. Sweden has been a leading country in school-based sexual and reproductive health (SRH) education for many years. Such education was previously offered at all levels in school, but nowadays it is only included in levels lower than high school. As a consequence this has led to insufficient knowledge about SRH among adolescents, and they are now requesting more information about reproduction and STIs.^25,26

Our study had limitations. There were fewer boys in CG1 than in CG2. If, in general, girls have better knowledge in this area, the total knowledge in CG1 would decrease if more boys were added. However, this would not affect the main results.

The response rate was low at follow-up. A total of 330 students were required to obtain a power of 80% but was not reached due to varying attendance of the students in the classroom on the day of data collection. Conclusions based on statistically significant differences between groups are unaffected while non-significant differences have to be cautiously interpreted due to lack of power.

Performing a large number of statistical tests increases the risk of mass significances. This risk was limited by a conservative interpretation of the analyses.

CONCLUSION

The baseline knowledge of HPV was very low among the 16-year-old students. Our study has shown that a short school-based intervention greatly can increase the students' knowledge about HPV, but that attitudes and behaviours are less easy to influence.

Footnotes

Acknowledgements

The study was funded by the Swedish Cancer Society (Cancerfonden) and The Jerring Foundation.

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