Vaccination against human papillomavirus in Brazilian schoolchildren: National Survey of School Health, 2019

Abstract Objective: to analyze the prevalence of schoolchildren vaccinated against human papillomavirus (HPV) and the reasons related to non-vaccination. Method: cross-sectional study, with data from the 2019 National Survey of School Health. The sample consisted of 160,721 students aged 13 to 17 years. The prevalence and confidence intervals (95%CI) of vaccinated adolescents were estimated according to location, sex, and administrative dependence of the school. The differences between the strata were evaluated with the Chi-square test. Adjusted prevalence ratios (aPR) and 95%CI were estimated with the Poisson regression model. Results: most of the students were vaccinated (62.9%), and the prevalence of girls (76.1%) was higher than that of boys (49.1%). The most prevalent reason for not vaccinating was “did not know they had to take” (46.8%), with the highest aPR in public schoolchildren in Brazil (1.6; 95%CI 1.5;1.7), from the Northeast region (1.2; 95%CI 1.1;1.2), and in students from private schools in the Northeast regions (1.1; 95%CI 1.1;1.2) and North (1.3; 95%CI 1.2;1.4). Conclusion: one out of every two Brazilian schoolchildren was vaccinated against HPV. Misinformation was a recurring reason for non-vaccination. The North and Northeast regions had the highest prevalence of non-vaccinated people, observed mainly in adolescents from public schools.


Participants
In this study, data from all schools and classes selected in the preparation stage of the research sampling plan were used. Participants were all students aged 13 to 17 years, enrolled from the 7 th grade of primary education to the 3 rd grade of secondary education, including technical courses with integrated high school and the regular/Teaching degree courses that were present on the day of data collection. Schools with less than 20 students enrolled, classes with a low number of valid questionnaires in relation to the total number of enrolled students, and questionnaires that did not meet the eligibility criteria previously established by the data collection team (12) were excluded from this study.

Study variables
The variables of this study were the HPV vaccination status of adolescents (evaluated by the question: were you vaccinated against the HPV virus? Answer options: yes or no) and the reasons for non-vaccination (assessed by the question: why were you not vaccinated against the HPV virus? Answer options: did not know they had to get immunized; distance or difficulty to go to the unit or service; fear of reaction to the vaccine; did not believe in the effect of the vaccine; mother, father, or guardian did not want to vaccinate him; another reason). In the PeNSE 2019 database, questions were selected that investigated whether the adolescent was adequately vaccinated against HPV and, if not, what was the reason for non-vaccination. The prevalence of each response was estimated according to the categories of analysis (location, sex, and administrative dependence of the school).

Bias control
Due to the complex sampling design of PeNSE and due to losses, post-stratification weights were considered for all analyses. Additionally, according to the IBGE publication, all research results went through a process of data evaluation and verification, in order to define which questionnaires would be considered as valid and, therefore, included in the research (12) .

Data processing and analysis
Initially, the prevalence of adolescents who answered on whether they were vaccinated against HPV was Rev. Latino-Am. Enfermagem 2022;30(spe):e3834. estimated, according to sex and administrative dependence of the school (public or private) with the respective 95% confidence interval (95%CI). Subsequently, the percentages of the reasons reported by the adolescents for not having vaccinated and the respective 95%CI were estimated, according to type of school administration (public or private) and location (region, federation units, and capitals) ( Figure 1).

Questions
Indicator and

Brazil, 2019
To evaluate the differences between the categories of analyses, estimates of 95%CI were considered, since the information returned by 95%CI is more valuable than the p-value (17) (18) . The adjustment was made since the literature reports that girls vaccinate more against HPV than boys (5) , making it possible to consider the influence of this sociodemographic factor (18) . To analyze the    25.4;27.9) and "fear of reaction to the vaccine" (7.7%; 95%CI 6.9;8.6), respectively ( Figure 3).  We noticed that aPR were higher among Brazilian schoolchildren from public schools for reasons related to "Did not know they had to get immunized" (1.6; 95%CI 1.5;1.7) and "Distance or difficulty to go to the unit or service" (1. aPR= Prevalence ratio adjusted for sex. 95%CI: 95% confidence interval. *Corresponds to the p-value of the aPR < 0.05, indicating statistically significant differences calculated by the Poisson regression model. Silva IAG, Sá ACMGN, Prates EJS, Malta DC, Matozinhos FP, Silva TMR As for the administrative dependence of the school, in addition to the answer "Did not know that they had to get immunized" (public school: 49.2%; 95%CI 47.6;50.9; private school: 31.4%; 95%CI 29.6;33.2), the answers "distance or difficulty to go to the unit or service" (4.2%; 95%CI 3.4;4.9) and "fear of reaction to the vaccine" (7.3%;95%CI 6.4;8.3) were more frequent in adolescent schoolchildren from public schools, while the answer "mother, father, or guardian did not want to vaccinate them" (14%; 95%CI 12.5;15.5) was more frequent in adolescents from private schools (Table 1).
Regarding the reasons, the answer "Did not know they had to get immunized" was more frequent in the

Discussion
Most of the schoolchildren aged 13 to 17 years who participated in PeNSE were vaccinated against HPV, with a higher prevalence of vaccination among girls than boys. In Brazil and in public schools of the Northeast region, the most frequent reason for non-vaccination was "Did not know they had to take it." In addition to this reason, the "distance or difficulty to go to the unit or service" was more frequent among adolescents enrolled in Brazilian public schools. Schoolchildren enrolled in In turn, having knowledge about the virus and about the action of the vaccine was a factor positively associated with vaccination of the adolescent public within national and international studies (5,25) . Regarding the source of information about HPV, a multicenter study with sexually active young adults recruited from 119 Primary Health Care (PHC) services revealed higher scores on knowledge about the virus among participants who were informed via health professionals and the media (23) . The research reinforced the importance of nurses working in these services of adopting communication strategies that favor the dissemination of information, favoring the adherence of this public to vaccination (21,26) .
Health professionals, in addition to providing information on HPV vaccination, should recommend it to adolescents (14,(21)(22)(23)(24)(25)(26) . Studies show that parents who received the recommendation from a health professional have a higher chance of reporting their intention to vaccinate their children when compared to parents who did not (14,26) . Another study, however, revealed that only 64.4% of the parents of girls and 41.6% of the parents of boys received recommendations from health professional regarding the vaccine (27) . Notably, a study conducted with nurses and other health professionals in Nigeria reported that knowledge about the HPV vaccine is favored by its recommendation to parents and adolescents (26) .
Considering that in our study most adolescents did not know that they had to be vaccinated and that there is evidence that knowledge about the vaccine is favored by its recommendation from a health professional (26) , strategies that prioritize the training of nurses on HPV prevention are necessary (26) , especially those who work in the vaccine rooms.
Regarding the administrative dependence of the school, there was a higher prevalence of adolescents enrolled in public schools who answered "did not know they had to take it." Another study, which analyzed data from the third edition of PeNSE 2015, also identified that in public schools there is a higher prevalence of unawareness about HPV vaccination (5) . Notably, of the HPV campaign (5) .
In addition to preventing cervical cancer, the HPV vaccine also prevents penile cancer and other types that affect individuals of both sexes (24) , which reinforces the importance of educating male adolescents and young adults on HPV vaccination. A study with PNI data also drew attention to the differences in HPV vaccine coverage in the female and male population (25) . In the  (19) .
The inadequate approach to sexual and reproductive rights associated with socially instituted differences contributes to the naturalization of the responsibility of female adolescents for the prevention of pregnancy, as well as for the prevention of sexually transmitted diseases, including HPV (29) . In this sense, in addition to knowing the factors that compromise the achievement of vaccine coverage goals, it is essential that nurses working in PHC services develop health strategies that reach adolescents and their families, adopting culturally appropriate, flexible methodologies that educate them on the importance of HPV vaccination (14) . in these regions (30) . In this sense, health strategies and policies are necessary to increase the support of the adolescent public living in these regions, especially in the Northeast, which has, in addition to the worst indicators of immunization against HPV (19) , the higher prevalence of cervical cancer and other neoplasms caused by the virus (24) .
In Brazil, regional inequalities in vaccination coverage are historical and significant, and the worst indicators of immunization are commonly identified within the States and municipalities of the North and Northeast regions, when compared to the South and Southeast regions (31)(32) . A national study that estimated the coverage of the first and second dose of the HPV vaccine in cohorts of girls aged 14, 15, and 16 years in 2017 (9) also identified heterogeneity of vaccination coverage, in addition to an association between the proportion of households without private bathrooms in the municipality and the worst indicators of immunization (9) . Also in this study, the States of Amazonas, Pará, Tocantins, Piauí, Paraíba, and Bahia, located in the North and Northeast regions, did not reach the goal of 80% of the vaccination coverage of the target population (9) .
We In this study, memory bias represented a limitation since adolescents had to evoke previous facts to answer questions from the PeNSE questionnaire.
Additionally, the target audience of the research tends to answer complex questions inaccurately, which may lead to underestimation or overestimation of the information provided (5) . The fear of judgment and feelings of shame from prior experience may prevent students from responding in a reliable way, representing a potential risk of obtaining inadequate information (25) . Considering the negative impacts Among these spaces, the school environment deserves attention for providing opportunities for the encounter and establishment of a communication channel favorable to clarifying doubts and addressing aspects potentially associated with HPV vaccine adherence, such as fear of adverse effects after vaccination and prevention of cervical cancer (5,(24)(25) .

Conclusion
The strengthening of public policies and health strategies, especially in the North and Northeast regions of the country, is essential to improve HPV vaccination indicators among the adolescent public. It is also worth mentioning the central role of nurses as a health educator, establishing a communication channel that provides information on vaccination against the virus, which can contribute to increased vaccination adherence among Brazilian adolescents.