Improvement of Parent’s Awareness, Knowledge, Perception, and Acceptability of HPV Vaccination After an Educational Intervention

Regardless of the disease burden of Human Papilloma Virus (HPV), the vaccine has not been included in the Indonesia National Immunization Program. Since 2017 there was a demonstration program of the HPV vaccination in Yogyakarta Province. This vaccine was given to female elementary school students in 5th and 6th grades. This study aimed to assess whether an educational intervention about the risks of HPV and the vaccine increases the parental awareness, knowledge, and perceptions toward HPV and the vaccine acceptability. study before the of after


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Background Globally, cervical cancer ranks the third most common cancer in women, with a total estimated 569,847 diagnosed cases of invasive cervical carcinoma with 311,365 deaths from the disease annually (1). In Indonesia, cervical cancer is the second most common cancer and the leading cause of death among women aged 15-40 years, with about 32,469 newly diagnosed cases annually (2). HPV infection occurs among the age of 15-59 years, and half of those cases occur within the age of 15-24 years, during the sexually active ages. Cervical cancer is linked to HPV infection. Low-risk types (HPV 6 and 11) can cause genital warts and low-grade cervical changes, whereas high-risk types (HPV 16 and 18) can cause highgrade cervical abnormalities that lead to cancers (3). The World Health Organization (WHO) recommended introducing HPV vaccination as part of a coordinated and comprehensive strategy to prevent cervical cancer and other diseases caused by HPV (4).
As one proactive way to increase HPV vaccine coverage, the Global Alliance for Vaccines and Immunization (GAVI) supports low-middle income countries in Southeast Asia, including Indonesia, to conduct the HPV Demonstration Program. This program was initiated in the provinces where the burden of cervical cancer cases was the highest and the provinces were ready to implement the HPV vaccination program. The rst place was in Jakarta Special Province (October 2016), and this effort was continued in the Special Region of Yogyakarta Province (2017), Surabaya (2018), Makassar (2019), and Manado (2019). The quadrivalent HPV vaccine was added to an existing school childhood immunization program (BIAS) for girl students of 5th (the rst dose) and 6th grade (the second dose) of elementary school. If the program is successful, then it will be an initial step to add the HPV vaccine into the National Immunization Program (NIP) (5). The WHO recommended 2 doses of HPV vaccine, explaining that a two-dose HPV vaccine schedule provides satisfactory immunological outcomes in adolescent girls less than 15 years old (6).
Because children in this age need parental consent for the vaccination, the acceptance of the HPV vaccine is highly dependent on the knowledge, perceptions, and approval of their parents (7), (8), (9). A systematic review found several factors associated with parents' acceptance of HPV vaccination for their children including: perceived susceptibility to HPV infection, bene ts of vaccination, the safety of the vaccine, social-environmental factors (e.g., social norms, media in uence, doctor's recommendation), and parental factors (educational level, household income, expenses, and attitudes) (10).
The WHO recommended countries which are introducing the HPV vaccine into their NIP should invest in a comprehensive communication plan to rst build community awareness and acceptance for the vaccine and the program. This plan includes clear program and communication objectives, understanding community knowledge, attitudes and practices, and de ned target audiences.
Communication efforts should reach all key target audiences, especially parents (11). Parents' misperceptions and concerns about the vaccine may affect their acceptance and coverage of the vaccine (12). Inadequate knowledge is one of the signi cant obstacles to increase HPV vaccine acceptability (13), (14). Prior studies in Indonesia reported that parents had a poor baseline knowledge about HPV infection, cervical cancer, and the HPV vaccine (15), (16). Educating parents was demonstrated to be an effective method to improve vaccine acceptability by increasing their knowledge and positive perceptions toward vaccination (17), (18).
To our knowledge, no study in Indonesia has assessed the impact of an education intervention on parental knowledge, perceptions, and acceptability of HPV vaccination. This study aimed to evaluate whether an educational intervention about HPV risks and the HPV vaccine increases the parental awareness, knowledge, and perceptions regarding HPV and the HPV vaccination acceptability.

Methods
We conducted a one group pre-test, post-test design study in Kulon Progo District, one of 2 districts in Yogyakarta Province, where the demonstration program was implemented, from July to August 2017, before the implementation of the HPV vaccination demonstration program. This research was part of a larger study assessing knowledge, perceptions, and acceptability of parents and teachers regarding HPV related to the disease and the vaccine. Parents of female elementary school students grades 5th and 6th were selected using a school-based proportional random sampling. A study information statement was sent to the parents, and they were invited to participate in the study. We excluded parents who cannot read and write.
After collecting socio-demographic and baseline data on knowledge, perceptions, and acceptability on HPV infection and the vaccine, an educational intervention was provided to the group of parents in the classroom. The intervention consists of a PowerPoint (PPT) presentation provided by a trained pediatric resident, followed by an interactive discussion. The session lasted around an hour. The presentation explained about HPV infection, cervical cancer, and HPV vaccination. The post-intervention data were collected immediately after the educational intervention. Data were collected using validated selfadministered questionnaires, which consisted of awareness (4 questions), knowledge and perceptions about HPV infection (14 and 6 questions), knowledge and perceptions about cervical cancer (3 and 2 questions), and knowledge and perceptions about HPV vaccination (5 and 2 questions). For the assessment of knowledge scores, if the answer was correct then it was given a value of 1 and if the answer was incorrect then a value of 0. Questions about perceptions used a 5-point Likert scale (ranging from strongly agree to strongly disagree). Acceptability was measured by a dichotomous item asking whether they would allow their daughters to receive the HPV vaccine, free of charge (yes or no). This questionnaire had been tested for validity and reliability. Ethical approval was attained from the Ethics Committee of the Faculty of Medicine, Public Health and Nursing, Universitas Gadjah Mada, Yogyakarta, Indonesia (KE/FK/0815/EC/2017). We obtained informed consent from all participants (parents). Participation was voluntary, and the responses were anonymous.
Descriptive statistics were used to describe the distribution, frequency, and percentage of variables. The statistical signi cance of the pre-/post-test intervention was assessed using McNemar and Wilcoxon Signed-Rank tests. Logistic regression analysis was used to determine the associations between potential predictors and vaccine acceptability. All analyses were performed with two-sided tests, and a value of p < 0.05 was considered signi cant.

Results
Of the 546 parents who were invited, 513 parents attended the educational intervention program (response rate was 94%), seven parents were excluded due to inability to read and write, resulting in a total data set of 506 participants. The majority of the respondents are mothers (92.8%), with a median age of 40 years, and the majority are Moslem (98.2%). Forty-three participants (8.8%) experienced a history of cancer in their family, and 4.4% mentioned that their daughter had already received the HPV vaccination (Table 1).  At baseline, the majority of parents already have a strong perception of the severity of cervical cancer. Most parents were "agree/strongly agree" that cervical cancer is a dangerous cancer (87.8%), and every woman was at risk of having cervical cancer (72.6%). However, the perception of the risk of having HPV infection was lower with only 40.3% aware. The perceptions of the bene t and safety of the HPV vaccine was high (78.6% and 69.7%, respectively) ( Table 3). Factors associated with HPV vaccine's acceptability after the intervention education In the bivariate analysis, we found that knowledge and perceptions of HPV infection, cervical cancer, and HPV vaccine were predictive of vaccine acceptability. There was no correlation between the sociodemographic characteristics of the respondents with HPV vaccination acceptability. In the multivariate analysis, we found that better knowledge of HPV vaccination and more positive perceptions of HPV vaccine were predictive of vaccine acceptability with OR 1.90 (95%CI:1.40-2.57) and OR 1.31(95%CI:1.05-1.63), respectively (Table 5).

Impact of the educational intervention program
After the educational intervention, there were signi cant improvements in parents' awareness, knowledge, and perceptions of HPV infection, cervical cancer, and the vaccine, p < 0.001 (Tables 2, 3   At the baseline, we found that most of our participants had heard about STIs and cervical cancer, but less than half of them had never heard about HPV infection and the vaccine. A previous qualitative study assessing parental knowledge and perceptions of HPV and cervical cancer prevention in rural Central Java, Indonesia (2015) found that most respondents have limited knowledge of HPV and the vaccine as well as the relationship between HPV and cervical cancer (15). Compared to a study 4-years earlier which was conducted in the same province (Yogyakarta Province) in 2013, there was almost no improvement in parental awareness of HPV vaccination (44% and 47%), and the percentage of parents who reported their children had received the vaccine (8.0% and 4.4%) (16). Since the vaccine has not been included in Indonesia NIP then this may be the reason why the community is not very aware of the availability of the vaccine and this causes the low vaccine uptake. These ndings are similar to previous studies in developing countries where HPV vaccination has not been included in their NIP (18), (19), (20).
Our study found that even before the educational intervention, parents already had a strong perception of the danger of cervical cancer. However, the perceptions of the susceptibility of HPV infection was considered low.
There were several factors related to the acceptability of HPV vaccination. From the regression analysis, we found that better knowledge and positive perceptions of the HPV vaccination were signi cantly associated with higher acceptability. In line with our study, previous reports have shown that parents' knowledge about HPV was positively correlated with HPV vaccination acceptability (9), (12). Perceived risks of HPV infection, perceived vaccine bene ts, and vaccine safety were associated with the acceptability of HPV vaccination. Perceptions that their children were at greater risk of getting cancer indicated more desire to permit their children to get the HPV vaccine. Parents wanting to protect their children from cervical cancer and other HPV related diseases as the perceived bene ts of HPV vaccination, had a strong relationship with the intention to vaccinate. On the other hand, parents who were not sure about HPV vaccine e cacy and afraid of any side effects which might be harmful to their children were less likely to accept the vaccine (21), (22), (23), (24), (25), (26).
We found that besides the vaccine's bene ts and safety, free of charge, the vaccine being included in NIP, and the vaccine considered halal (permissible under Islamic Shariah Law) were important considerations for accepting the vaccine. Including HPV vaccine in the NIP and providing health insurance could eliminate the cost barriers. Because the majority of our study population is Muslim, the halal issue is an important consideration for accepting the vaccine. Previously, the non-halal status was reported as a barrier to the rotavirus vaccine acceptability in Yogyakarta, Indonesia. Engagement of religious leaders is needed to facilitate the bridge between immunization programs and the community, particularly during the introduction of a new vaccine (27).
Earlier studies found that parents need HPV-related information to decide whether to accept or refuse the HPV vaccination (8), (13), (28). In line with the WHO recommendations (11), a systematic review of knowledge, attitudes, and barriers toward HPV vaccination in developing economic countries of South-East Asia Region emphasized the importance of educational campaigns before the vaccine is included in the NIP to improve vaccine uptake (21). Parents should be provided with more detailed information about HPV infection, cervical cancer, and HPV vaccination, which would help parents avoid any misunderstandings and to change parents toward a positive attitude. In line with previous studies, our study found that a structured education program improved parent's knowledge, and perception as well as their acceptability. A one-hour educational presentation was effective in improving parent's knowledge and had an important impact on vaccine acceptance (29). A study in China indicated that health educational seminars could effectively increase the parental knowledge level about vaccinations (17). A school-based intervention study assessed the effect of an hour PPT presentation/educational intervention on HPV knowledge and attitudes towards HPV and its vaccine among junior school students in Chengdu, China. The results of the study demonstrated the effectiveness of this intervention in improving HPV knowledge among students and in increasing their willingness to be vaccinated (30).
The educational intervention conducted in our study, in the form of a presentation by professional health educators, was shown to signi cantly improve the parents' knowledge and perceptions about HPV. Giving educational campaigns could increase parental knowledge and perceptions about HPV, concurrently with physician recommendations and nationally funded vaccination programs (20). A systematic scoping review (2019) regarding communication concerning HPV vaccinations in low and middle-income countries found that physicians were important components to deliver information about HPV and give parents a recommendation to get HPV vaccination for their children (22). Another systematic review conducted by Radisic et al. (2017) found that uptake of HPV vaccination may be facilitated by encouraging health care provider endorsement (10).
This research has some limitations. First, this one group pre-test -post-test design study without a control group did not allow us to con rm any causal relations between the intervention and outcomes. A pre-and post-test without follow-up also could not determine the long-term effectiveness of the educational intervention on HPV vaccination acceptability. Further studies with longer follow-up are needed to evaluate the long-term and actual effectiveness of improving parents' knowledge and perceptions about the HPV vaccination. The strength of this study is that it assessed the effectiveness of an education intervention before the implementation of the HPV vaccination demonstration program, which included a representative sample of parents in the Kulon Progo District. The results of this study can provide important evidence to the policy-makers about the importance of health education.

Conclusion
Parental knowledge and perceptions toward HPV and the vaccine was considered insu cient. A structured educational intervention program conducted by quali ed health providers is effective in improving parental awareness, knowledge, and perceptions toward HPV as well as the acceptability of the vaccine. There was a signi cant correlation between improving the parental knowledge and perceptions of HPV vaccine with increasing acceptability of the HPV vaccine. Availability of data and materials The datasets generated and/or analysed during the current study are not publicly available but are available from the corresponding author on reasonable request.