ABSTRACT
Background: Willingness to be vaccinated with human papillomavirus (HPV) vaccine among junior middle school students in China is not well understood. We conducted a cross-sectional study to assess awareness of HPV and the HPV vaccine and explore the factors associated with willingness to be vaccinated. Methods: First-year students from two junior middle schools in Jinan, China were selected by cluster sampling on December 28, 2015, December 26, 2016, and January 11, 2017, and a self-administered questionnaire was used to collect information. Multivariate logistic regression was conducted to explore the factors associated with willingness to be vaccinated with the HPV vaccine. Results: A total of 1021 junior middle school students participated in this survey. Only 15.5% of them had heard of HPV and 18.9% of them had heard of the HPV vaccine. Students who were willing to take the HPV vaccine in the future accounted for 66.9%. Factors associated with the HPV vaccination were: urban junior middle school students (AOR: 1.51, 95% CI: 1.09–2.09), female students (AOR: 1.90, 95% CI: 1.36–2.66), students surveyed in 2015 (AOR: 1.69, 95% CI: 1.26–2.28), regarding menstruation/spermatorrhoea as a normal physiological phenomenon (AOR: 1.64, 95% CI: 1.14–2.36), believing vaccination is an important way to prevent diseases (AOR: 1.36, 95% CI: 1.01–1.83), believing that the first vaccination should be in infancy (AOR: 1.41, 95% CI: 1.04–1.92), believing that cervical cancer is a concern for themselves (AOR: 1.95, 95% CI: 1.28–2.97), and having heard of HPV (AOR: 1.84, 95% CI: 1.13–2.98). Conclusions: Awareness of HPV and the HPV vaccine among junior students was low, however willingness to be vaccinated was high. Education focusing on HPV-related knowledge in addition to sex education is needed to promote the coverage of the HPV vaccine.
KEYWORDS: human papillomavirus (HPV), willingness to be vaccinated, middle school students, vaccine, sex education
Background
Cervical cancer is the fourth most common cancer in women worldwide, and the second most common in developing countries, with approximately 527,600 new cases and 265,700 deaths over the world in 2012.1 China has a high burden of cervical cancer and disparities existing among different regions.2 The cervical cancer mortality in China has increased from 1.22/105 in 2003 to 2.59/105 in 2011, and the steady incidence increase will continue in the next 5 years.3 According to cancer statistic in China, an estimation of 98,900 new cervical cancer cases and 30,500 deaths was recorded in 2015.4 So it is necessary to take measures to control and reduce the health burden of cervical cancer.
HPV is the most common sexually transmitted infection worldwide. Persistent high-risk HPV infection contributes to the development of cervical cancers and HPV is found in 99.7% of all cervical cancer during the 1990s.5,6 HPV 16 and 18 are responsible for about 70% of invasive cervical cancer cases worldwide.7 Vaccination is an effective method to prevent diseases. The first vaccine against HPV, Gardasil, was licensed by the U.S. Food and Drug Administration (FDA) in June 2006.8 It is a quadrivalent vaccine against HPV type 16 and 18, and also targets HPV6 and HPV11 which caused at least 80% of genital warts.9 Cervarix, a bivalent HPV vaccine was approved in 2009. Prophylactic HPV vaccines have excellent efficacy in preventing cervical cancer.10,11 The most recent, a nine-valent HPV vaccine was approved in December 2014, which could improve the efficacy of the quadrivalent vaccine from 70% to 90% for cervical cancer.12
Since 2006, national immunization policies for HPV have been adopted in many countries. As of the middle of 2015, 65 countries had put HPV vaccines on their national immunization schedule.13 Although two vaccines had been available in Hong Kong since 2009, it was not until July 2016 that the China Food and Drug Administration approved the bivalent vaccine Cervarix produced by GlaxoSmithKline.
Studies have shown that vaccination of HPV is most effective to be administered before sexual debut.14 According to a meta-analysis, the average age of beginning sexual activity of Chinese females was 19.4(±1.9) years,15 and another study carried out in Wuhan showed the mean age of sexual debut was 19.3(±1.7) years.16 A multi-center study reported that the majority of females in mainland China had sexual debut at age of over16 years, suggesting that HPV vaccination in China should be implemented between 13 of 15 years of age, before the completion of national compulsory education.17 Therefore the target population for HPV vaccination on the Chinese mainland should be junior middle school students.
The successful introduction of the HPV vaccine depends on a range of factors, such as socio-demographic factors, awareness and knowledge of HPV infection, as well as vaccination willingness. Studies on awareness regarding HPV infection and attitudes towards HPV vaccination have been conducted in many countries from the perspectives of physicians, parents, and adolescents.18–20 In China, researchers have investigated college students and parents for their awareness of the HPV vaccine and future vaccine uptake.21–24 As the HPV vaccine has only been recently introduced in China, studies exploring willingness to be vaccinated among the target population are necessary. They are important to make policies on how the HPV vaccination should be applied to the cervical cancer control program.
The purpose of this study was to assess awareness of HPV and the HPV vaccine and willingness to be vaccinated among junior middle school students in Jinan, China, as well as to explore the factors associated with the HPV vaccination, and then to provide advice for the promotion of the HPV vaccination in mainland China in the future.
Results
Demographic characteristics of participants
A total of 1083 students were approached and 1029 of them participated in this study. The response rate was 95.0%. Eight were excluded from the analysis because they completed less than 60% of the questions. As a result, a total of 1021 questionnaires were used for analysis. Demographic characteristics of the participants are presented in Table 1. Of the participants, 666 (65.2%) were from the urban middle school (348 males and 301 females, with 17 missing values) and 355 (34.8%) were from the rural middle school (188 males and 157 females, with 10 missing values). The average age of participants was 12.32 years (SD = 0.51). The majority (97.7%) of the students were Han Chinese.
Table 1.
Demographic characteristics of study participants (N = 1021).
| Variables | Number | Percentage |
|---|---|---|
| School type | ||
| Urban middle school | 666 | 65.2% |
| Rural middle school | 355 | 34.8% |
| Survey year | ||
| 2015 | 536 | 52.5% |
| 2016 | 485 | 47.5% |
| Gender* | ||
| Male | 536 | 53.9% |
| Female | 458 | 46.1% |
| Race* | ||
| Han | 971 | 97.7% |
| Other | 23 | 2.3% |
Numbers do not add up to 1021 due to missing data.
Perceptions of vaccines in general
In our study, female students were more obedient to parents compared with male students when making the vaccination decision (76.8% vs 69.3%, P = 0.002). There were 80.9% of students who thought prevention was better than treatment for any diseases. Among all students, 55.8% agreed that vaccination was an important means of preventing disease, and it was found associated with gender, with more males responded opted yes to this statement than females (60.0% vs 50.9%, P = 0.004). About two-thirds (65.8%) of students believed that the first vaccination should be in infancy, whereas 18.1% chose childhood. There were 1.9% of students who thought that vaccines were useless and 2.8% thought that vaccines were needed only after becoming sick. See Table 2 for details.
Table 2.
Perception of vaccines among junior middle school students in Jinan, China (N = 994).
| Items | Male students (%) | Female students (%) | Total (%) | P |
|---|---|---|---|---|
| Whose opinion do you value most about vaccination | 0.002 | |||
| Parents | 339(69.3) | 324(78.6) | 663(73.6) | |
| Others | 150(30.7) | 88(21.4) | 238(26.4) | |
| Prevention is better than treatment | 0.621 | |||
| Yes | 437(82.1) | 369(80.9) | 806(81.6) | |
| No | 95(17.9) | 87(19.1) | 182(18.4) | |
| Vaccination is an important means of preventing disease | 0.004 | |||
| Yes | 319(60.0) | 232(50.9) | 551(55.8) | |
| No | 213(40.0) | 224(49.1) | 437(44.2) | |
| The first vaccination should be in infancy | 0.022 | |||
| Yes | 333(62.6) | 317(69.5) | 650(65.8) | |
| No | 199(37.4) | 139(30.5) | 338(34.2) | |
| The first vaccination should be in childhood | 0.079 | |||
| Yes | 107(20.1) | 72(15.8) | 179(18.1) | |
| No | 425(79.9) | 384(84.2) | 809(81.9) | |
| Vaccine is useless | 0.721 | |||
| Yes | 11(2.1) | 8(1.8) | 19(1.9) | |
| No | 521(97.9) | 448(98.2) | 969(98.1) | |
| Vaccination should only be given after becoming ill | 0.023 | |||
| Yes | 21(3.9) | 7(1.5) | 28(2.8) | |
| No | 511(96.1) | 449(98.5) | 960(97.2) |
Note: The chi-square test was used and P<0.05 was considered as statistically significant. The total number varies due to the missing values.
Knowledge and perceptions of HPV and the HPV vaccine
More female students had heard of cervical cancer than had male students (43.8% vs 28.1%, P<0.001). Of the participants, 44.3% of female students and 8.5% of male students believed that cervical cancer is a concern for themselves. Only 15.5% of participants had heard of HPV and 18.9% had heard of the HPV vaccine. Among the students who had heard of the HPV vaccine, 38.6% knew that the HPV vaccine can effectively prevent cervical cancer, anal cancer, and genital warts and 31.9% had inquired about the HPV vaccine. Female students were more willing to take the HPV vaccine than male students (76.7% vs 58.6%, P<0.001). See more details in Table 3.
Table 3.
Perception of HPV/HPV vaccine among junior middle school students in Jinan, China (N = 994).
| Items | Male students (%) | Female students (%) | Total (%) | P |
|---|---|---|---|---|
| Heard of cervical cancer | 0.000 | |||
| Yes | 149(28.1) | 200(43.8) | 349(35.4) | |
| No | 381(71.9) | 257(56.2) | 638(64.6) | |
| Cervical cancer is a concern for myself | 0.000 | |||
| Yes | 45(8.5) | 198(44.3) | 243(24.8) | |
| No | 486(91.5) | 249(55.7) | 735(75.2) | |
| Heard of HPV | 0.684 | |||
| Yes | 85(15.9) | 68(15.0) | 153(15.5) | |
| No | 449(84.1) | 386(85.0) | 835(84.5) | |
| Heard of the HPV vaccine | 0.672 | |||
| Yes | 102(19.4) | 83(18.4) | 185(18.9) | |
| No | 423(80.6) | 369(81.6) | 792(81.1) | |
| Know that the HPV vaccine can prevent cervical cancer/anal cancer/genital warts* | 0.507 | |||
| Yes | 38(40.9) | 28(35.9) | 66(38.6) | |
| No | 55(59.1) | 50(64.1) | 105(61.4) | |
| Prior consultation regarding HPV vaccine information* | 0.388 | |||
| Yes | 31(34.8) | 22(28.6) | 53(31.9) | |
| No | 58(65.2) | 55(71.4) | 113(68.1) | |
| Willing to take the HPV vaccine | 0.000 | |||
| Yes | 310(58.6) | 345(76.7) | 655(66.9) | |
| No | 220(41.4) | 104(23.3) | 324(33.1) |
Only students who have heard of the HPV vaccine answered these questions.
Note: The chi-square test was used and P<0.05 was considered as statistically significant. The total number varies due to the missing values.
Factors associated with the willingness to be vaccinated for HPV
As shown in Table 4, eight variables were found associated with willingness to be vaccinated in the multivariate logistic regression analysis. Students from the urban junior middle school were more willing to get vaccinated (AOR: 1.51, 95% CI: 1.09–2.09). Female students were more tended to take vaccination (AOR: 1.90, 95% CI: 1.36–2.66). Students who were surveyed in 2015 were more willing to take the vaccine (AOR: 1.69, 95% CI: 1.26–2.28). In addition, students who regarded menstruation/spermatorrhoea as a normal physiological phenomenon were more willing to take HPV vaccine (AOR: 1.64, 95% CI: 1.14–2.36). Students who thought that vaccination is an important means of preventing disease (AOR: 1.36, 95% CI: 1.01–1.83) or thought that the first vaccination should be in infancy (AOR: 1.41, 95% CI: 1.04–1.92) were more willing to take the HPV vaccine. Students who concerned about cervical cancer were more willing to take the vaccine (AOR: 1.95, 95% CI: 1.28–2.97), and students who had heard of HPV had a higher willingness to be vaccinated (AOR: 1.84, 95% CI: 1.13–2.98).
Table 4.
Factors associated with willingness to be vaccinated with the HPV vaccine among junior middle school students in Jinan, China.
| Variables | OR (95%CI) | P | AOR (95%) | P |
|---|---|---|---|---|
| School type | ||||
| Urban | 1.99(1.52–2.61) | 0.000 | 1.51(1.09–2.09) | 0.014 |
| Rural | Ref | Ref | ||
| Gender | ||||
| Male | Ref | 0.000 | Ref | 0.000 |
| Female | 2.35(1.78–3.11) | 1.90(1.36–2.66) | ||
| Year | ||||
| 2015 | 1.54(1.18–2.00) | 0.001 | 1.69(1.26–2.28) | 0.001 |
| 2016 | Ref | Ref | ||
| Received sexual education/knowledge | ||||
| Yes | 1.61(1.23–2.10) | 0.000 | ||
| No | Ref | |||
| How well do you know adolescent sexual health | ||||
| Very well | 2.56(1.43–4.60) | 0.002 | ||
| Well | 2.64(1.68–4.14) | 0.000 | ||
| A little | 2.49(1.63–3.82) | 0.000 | ||
| I do not know | Ref | |||
| Menstruation/spermatorrhea is a normal physiology phenomenon | ||||
| Yes | 2.69(1.98–3.64) | 0.000 | 1.64(1.14–2.36) | 0.005 |
| No/not sure | Ref | Ref | ||
| Vaccination is effective in preventing diseases | ||||
| Yes | 1.33(1.02–1.73) | 0.035 | 1.36(1.01–1.83) | 0.046 |
| No | Ref | Ref | ||
| The first vaccination should be in infancy | ||||
| Yes | 1.81(1.38–2.39) | 0.000 | 1.41(1.04–1.92) | 0.027 |
| No | Ref | Ref | ||
| Vaccine is useless | ||||
| Yes | 0.386(0.15–0.99) | 0.047 | ||
| No | Ref | |||
| Heard of cervical cancer | ||||
| Yes | 2.12(1.58–2.85) | 0.000 | ||
| No | Ref | |||
| Cervical cancer is relative to me | ||||
| Yes | 3.01(2.08–4.34) | 0.000 | 1.95(1.28–2.97) | 0.002 |
| No | Ref | Ref | ||
| Heard of HPV | ||||
| Yes | 2.07(1.37–3.14) | 0.001 | 1.84(1.13–2.98) | 0.014 |
| No | Ref | Ref | ||
| Heard of the HPV vaccine | ||||
| Yes | 1.73(1.20–2.50) | 0.003 | ||
| No | Ref | |||
| Know that the HPV vaccine can prevent cervical cancer/anal cancer/genital warts | ||||
| Yes | 2.50(1.29–4.86) | 0.007 | ||
| No | Ref | |||
| Prior consultation regarding HPV vaccine information | ||||
| Yes | 1.97(1.00–3.88) | 0.049 | ||
| No | Ref |
Note: All factors in the table were variables with P<0.10 in univariate logistic regression models. Variables with AOR in the table were variables that eventually entered the multivariable logistic regression model. OR, odds ratio; AOR, adjusted odds ratio; 95%CI, 95% confidence interval.
Discussion
In this study, we assessed awareness of cervical cancer, HPV, and the HPV vaccine and willingness to be vaccinated with the HPV vaccine among junior middle school students in Jinan, China and explored the factors associated with willingness to be vaccinated. It was found that the junior middle school students’ awareness of HPV and the HPV vaccine was low, and awareness rate of the HPV vaccine was similar to a meta-analysis which reported a rate of 15.95% in China.23 However, awareness rate of HPV among teenagers in China was lower than that of adolescents in other countries.25–27 Our study showed that there was no sex difference between males and females with regarding to having heard of HPV or the vaccine. This could be explained by the following reasons: a) the HPV vaccine was introduced in China in July 2016 and was not yet put on the market, thus only a small number of people had heard of it. b) According to the teachers in both middle schools, they had not learned about HPV and there was no special course related to HPV for girls. Based on experiences, parents are less likely to talk about HPV with their children of this age. They may have heard about HPV or the HPV vaccine from TV or Internet, therefore the opportunities to access related information for females and males were same. Although awareness of the HPV vaccine was low, willingness to be vaccinated was high, 66.9% of participants would take the HPV vaccine. A similar result was reported in a study among college students in China,22 in which only 5.4% of college students had heard of the HPV vaccine whereas 70.6% were willing to take the HPV vaccine. This high vaccination willingness could be explained by the positive attitudes of students towards vaccines. The students regarded vaccination as an effective way to prevent disease so that they were willing to take the vaccine even though they did not know much about it.
We found that urban junior middle school students were more willing to take vaccine than those in the rural middle school. Few studies considered urban/rural as a predictor of willingness to be vaccinated, although some studies included income.28,29 There is a possibility that rural junior school students were less willing to take the vaccine due to family income, however further research is needed to support this conjecture. Students surveyed in 2016 were less willing to take the vaccine than those in 2015, which was opposite to our expectation. One possible reason is that students surveyed in 2016 knew that the vaccine had been recently licensed, they may have been concerned about the safety and side effects of the vaccine in the Chinese population.
Female students seemed to be more willing to take the HPV vaccine, which is in accordance with the result of other studies.30–32 About 40% of male students in our study would not take the HPV vaccine. They may have thought that the HPV vaccine is only related to females as the Chinese name of the HPV vaccine sounds like “breast” in Chinese. There were only 8.5% of male students thought that cervical cancer is a concern for themselves. Possible reasons might be that those male students did not understand what cervical cancer is, or they knew the fact that their partner will have a possibility of getting cervical cancer if they were infected. In addition, only 38 male students knew that the HPV vaccine could prevent not only cervical cancer but also anal cancer and genital warts. An information intervention study was carried out on male university students, participants who received the intervention emphasizing both altruistic motives and male-specific information had the greatest vaccine acceptance.33 Therefore, education with emphasis on male-specific HPV-related illnesses and vaccine benefits is needed in order to enhance HPV vaccine uptake among male students.
China has relatively conservative cultural tradition. Vaccination with a vaccine that can prevent cervical cancer and genital diseases caused by sexually transmitted infections may be a sensitive topic. Adolescents’ sexual knowledge was included in our research as a factor that may influence the promotion of the HPV vaccine. Students who regarded menstruation / spermatorrhea as normal physiological phenomenon were more willing to get vaccinated, which indicated that students with better sexual health knowledge had higher intention of being vaccinated. A study conducted among Chinese international students suggested that the HPV vaccine should be further promoted alongside sex education.34 Participants in that study felt resistant to HPV vaccination and linked HPV infection to promiscuous sexual behavior and infidelity when they knew that HPV is transmitted by sexual contact, however further in depth knowledge could reduce stigmas related to HPV infection. Hence HPV vaccination programs should not only cover knowledge about HPV but also pay more attention to sex education to eliminate misconceptions.
In this study, students who believed that vaccination is important for preventing diseases and that the first vaccination should be in infancy showed higher willingness to be vaccinated than those who did not, indicating that a better understanding about vaccines is associated with higher vaccination willingness. Emphasis must be placed on the prophylactic nature of vaccines and the importance of adolescent vaccination.
This study showed that having heard of HPV was a determinant of HPV vaccination, although different results were reported in other studies,35,36 in which awareness of HPV was not associated with vaccine acceptance. Previous researches proved that increased knowledge of HPV and the HPV vaccine had positive effect on willingness to be vaccinated. Adolescent girls in Hong Kong had increased intention to vaccination after an education program.37 Lecture-based education was also proved to be effective among employed female and female undergraduate students on the Chinese mainland.38 Willingness to be vaccinated was higher in students who believed that cervical cancer is a concern for themselves. This is consistent with a study carried out among parents of young adolescents in China, which found that fear of cervical cancer was positively associated with vaccine uptake.39 Fear of cervical cancer was also the main reason for making the decision to be vaccinated among Indonesia parents and Swedish women.40,41 Further efforts are needed to promote the understanding of HPV infection and of the benefits of HPV vaccines.
Government policies and mandates may lead to improved HPV vaccination and universal HPV vaccine programs should be established since the vaccine is now approved. Our result highlighted the need for further education on HPV infection and associated diseases with the aim of increasing the level of knowledge. The government should make full use of the schools as an important resource of informing adolescent students about vaccine related health issues. Besides, including the HPV vaccine in the expanded immunization plan and financial support would be good for HPV vaccination.39 Local health departments should provide education on the benefits of HPV vaccination and explore the demand of the HPV vaccine to obtain higher coverage of vaccination. Furthermore, healthcare providers are very influential for HPV vaccine uptake. Recommendations from healthcare providers may have a positive influence on decision making.21,42 As healthcare providers must be at the forefront of education and advocacy for HPV vaccination, they need to be trained to communicate about HPV and the vaccine more effectively. It is noteworthy that even junior middle school students were willing to be vaccinated, they will not certainly get vaccinated in the future, because the social structure in China will not permit vaccination of this age-group without parental approval. Nevertheless, it is still necessary to improve awareness of HPV vaccines for junior middle school students. Children's opinions also matter in their parents’ decision-making and increasing student's knowledge of the HPV vaccine will enhance the knowledge of parents to some degree as well.
There were some limitations in this study though. First, it was a cross-sectional study. Caution should be taken when interpreting the findings in our study owing to the cross-sectional nature that prevents us from making any statements regarding causality. Second, the participants were selected by convenience sampling rather than random sampling, and consequently the study population is not optimally representative. Third, we did not determine the validity and reliability of the questionnaire. Finally, the study was a preliminary exploration and some detailed information such as the knowledge level of HPV and reasons for refusing HPV vaccine were not collected. For future study on this topic on the Chinese mainland, it would be better to include this information.
In conclusion, awareness of HPV and HPV vaccine among junior middle school students in Jinan was low. However, the attitude towards future vaccination was encouraging. Efforts should be made to improve awareness and knowledge of HPV and the HPV vaccine and cervical cancer among junior middle school students. Since the adolescent's sexual knowledge was poor, sex education should include HPV vaccine promotion. Education programs that emphasize the role of vaccines in preventing diseases and improve the knowledge of HPV and HPV vaccine are necessary to extend the coverage of vaccination programs.
Materials and methods
Study population
Jinan is located in the middle west of Shandong Province and is the provincial capital. The study was conducted in two junior middle schools in Jinan, which were selected for convenience. One is an urban school and the other is a rural school. The urban school is located in the downtown and the majority of students in this school are children of university teachers. The rural school is located in a suburban district, and students are migrant workers' children. First-year students from those two schools were selected by cluster sampling. In the urban middle school, 7 out of 10 classes were selected in 2015 and 6 out of 11 classes were selected in 2017. In the rural school, 4 out of 6 classes were selected both in 2015 and 2016.
The study was approved by the Ethical Review Committee (ERC) of School of Public Health in Shandong University. Informed consent was obtained from each participant prior to our survey.
Data collection
The survey was administered on December 28, 2015, December 26, 2016, and January 11, 2017. Our questionnaire was self-developed and administered in Chinese. It consisted of questions about socio-demographic characteristics, knowledge of adolescent sexual health and general knowledge of vaccines, HPV and the HPV vaccine, and willingness to be vaccinated with the HPV vaccine. Data was collected as follows:
-
1)
Socio-demographic information collected included: school, gender, age, and race.
-
2)
Perception of adolescent sexual health: Students were asked ‘Have you received sex education?’ and those who answered yes needed to answer when was the first time they received it. Students were asked ‘How well do you know adolescent sexual knowledge’ with four options (very well/ well/ a little/ none) and students who responded ‘very well’ should correctly understand the physical and psychological changes during adolescence and how to treat these changes properly. Then they were asked about their attitude towards puppy love and ‘Do you think menstruation or spermatorrhoea is a normal physiological phenomenon?’ with the option of yes, no, and do not know. This was recorded as ‘yes’ (original ‘yes’) and ‘no/do not know’ (combined ‘no’ and ‘do not know’) in the analysis.
-
3)
Perception of vaccines in general and knowledge of the HPV vaccine: Students were asked whose opinion they valued most about vaccination. Then six comments were listed about general vaccines and students were asked to choose all the comments they agreed with. Then students were asked ‘Had you heard of cervical cancer / HPV /HPV vaccine before the survey?’ and ‘Do you think cervical cancer is a concern for yourself?’ Students who reported that they had heard of the HPV vaccine also needed to answer, ‘Do you know that HPV vaccines are effective in preventing cervical cancer / anal cancer / genital warts?’ and ‘Did you have prior consultation regarding HPV vaccine information?’ Finally, students were asked ‘Will you take the HPV vaccine if it is available?’
The junior middle school students were informed of the purpose and procedure of this study at the beginning and participation in this study was voluntary. Students who signed the informed consent completed an anonymous self-administered questionnaire with the help of trained research investigators. Questionnaires with incomplete items >40% and/or logic errors were excluded.
Statistical analysis
Frequency and percentage was used to describe the characteristics of participants, attitudes towards vaccines in general, awareness of HPV and the HPV vaccine, and willingness to be vaccinated. The chi-square test was used to analyze the difference between male students and female students. P < 0.05 was considered as statistically significant. Univariate logistic regression was used to evaluate the factors associated with willingness to be vaccinated with the HPV vaccine. Variables with P value <0.1 were entered into a multivariate logistic regression model, in which adjusted odds ratio (AOR) and 95% confidence intervals were calculated. A stepwise approach was done in the multivariate logistic regression model.43 Missing data was excluded in the analysis. SPSS 20.1 software was used for analysis.
Supplementary Material
Disclosure of potential conflicts of interest
The authors reported no conflict of interest.
Acknowledgments
We thank the middle schools involved in this survey and students who helped to complete the survey questionnaires. Thanks to Dr. Edward C. Mignot, and Ms. Aifeng Liu, Shandong University, for linguistic advice.
Funding
This study was funded by Project HOPE and Cancer Foundation of China “Cervical Cancer and HPV Infection Prevention Health Education Program”. The funder did not participate in any part of the study from design to approval of the manuscript, except for supporting this project.
Authors’ contributions
XZ, FZ, YQ, WM, and LG were involved in the conception and design of the study. LX, WH, HZ, and ZX acquired the data. LX conducted, analyzed, and interpreted the results. LX and WM were involved in drafting the manuscript and made critical revision of the manuscript for important intellectual content. All authors read and approved the manuscript.
References
- 1.Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics, 2012. CA Cancer J Clin. 2015;65:87–108. doi: 10.3322/caac.21262. PMID:25651787 [DOI] [PubMed] [Google Scholar]
- 2.Di J, Rutherford S, Chu C. Review of the Cervical Cancer Burden and Population-Based Cervical Cancer Screening in China. Asian Pacific journal of cancer prevention: APJCP. 2015;16:7401–7. doi: 10.7314/APJCP.2015.16.17.7401. PMID:26625735 [DOI] [PubMed] [Google Scholar]
- 3.Du PL, Wu KS, Fang JY, Zeng Y, Xu ZX, Tang WR, Xu XL, Lin K. Cervical Cancer Mortality Trends in China, 1991–2013, and Predictions for the Future. Asian Pacific journal of cancer prevention: APJCP. 2015;16:6391–6. doi: 10.7314/APJCP.2015.16.15.6391. PMID:26434848 [DOI] [PubMed] [Google Scholar]
- 4.Chen W, Zheng R, Baade PD, Zhang S, Zeng H, Bray F, Jemal A, Yu XQ, He J. Cancer statistics in China, 2015. CA Cancer J Clin. 2016;66:115–32. doi: 10.3322/caac.21338. PMID:26808342 [DOI] [PubMed] [Google Scholar]
- 5.Walboomers JM, Jacobs MV, Manos MM, Bosch FX, Kummer JA, Shah KV, Snijders PJ, Peto J, Meijer CJ, Munoz N. Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol 1999;189:12–9. doi: 10.1002/(SICI)1096-9896(199909)189:1%3c12::AID-PATH431%3e3.0.CO;2-F. PMID:10451482 [DOI] [PubMed] [Google Scholar]
- 6.Bosch FX, Lorincz A, Munoz N, Meijer CJ, Shah KV. The causal relation between human papillomavirus and cervical cancer. J Clin Pathol. 2002;55:244–65. doi: 10.1136/jcp.55.4.244. PMID:11919208 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Clifford G, Franceschi S, Diaz M, Munoz N, Villa LL. Chapter 3: HPV type-distribution in women with and without cervical neoplastic diseases. Vaccine. 2006;24 Suppl 3:S3/26–34. doi: 10.1016/j.vaccine.2006.05.026 PMID:16950015 [DOI] [PubMed] [Google Scholar]
- 8.Speck LM, Tyring SK. Vaccines for the prevention of human papillomavirus infections. Skin Therapy Lett. 2006;11:1–3. PMID:16912836 [PubMed] [Google Scholar]
- 9.Koutsky LA. Prevention of HPV-related cancers through immunization. Paper presented at: 5th AACR International Conference on Frontiers in Cancer Prevention Research, Boston, Massachusetts, November 12–15, 2006. [Google Scholar]
- 10.Garland SM, Hernandez-Avila M, Wheeler CM, Perez G, Harper DM, Leodolter S, Tang GW, Ferris DG, Steben M, Bryan J, et al.. Quadrivalent vaccine against human papillomavirus to prevent anogenital diseases. N Engl J Med. 2007;356:1928–43. doi: 10.1056/NEJMoa061760. PMID:17494926 [DOI] [PubMed] [Google Scholar]
- 11.Munoz N, Kjaer SK, Sigurdsson K, Iversen OE, Hernandez-Avila M, Wheeler CM, Perez G, Brown DR, Koutsky LA, Tay EH, et al.. Impact of human papillomavirus (HPV)-6/11/16/18 vaccine on all HPV-associated genital diseases in young women. J Natl Cancer Inst. 2010;102:325–39. doi: 10.1093/jnci/djp534. PMID:20139221 [DOI] [PubMed] [Google Scholar]
- 12.Fait T, Dvorak V, Pilka R. Nine-valent HPV vaccine–new generation of HPV vaccine.. Ceska Gynekol. 2015;80:397–400. PMID:26741152 [PubMed] [Google Scholar]
- 13.Brotherton JML, Bloem PJN. HPV Vaccination: Current Global Status. Current Obstetrics & Gynecology Reports. 2015;4:220–33. doi: 10.1007/s13669-015-0136-9. [DOI] [Google Scholar]
- 14.Erickson BK, Landers EE, Huh WK. Update on vaccination clinical trials for HPV-related disease. Clin Ther. 2014;36:8–16. doi: 10.1016/j.clinthera.2013.11.003. PMID:24417781 [DOI] [PubMed] [Google Scholar]
- 15.Yu XM, Guo SJ, Sun YY. Sexual behaviours and associated risks in Chinese young people: a meta-analysis. Sexual Health. 2013;10:424–33. doi: 10.1071/SH12140. PMID:23962473 [DOI] [PubMed] [Google Scholar]
- 16.Li J, Li S, Yan H, Xu D, Xiao H, Cao Y, Mao Z. Early sex initiation and subsequent unsafe sexual behaviors and sex-related risks among female undergraduates in Wuhan, China. Asia-Pacific journal of public health / Asia-Pacific Academic Consortium for Public Health. 2015;27:21s−9s. doi: 10.1177/1010539514549186. [DOI] [PubMed] [Google Scholar]
- 17.Zhao FH, Tiggelaar SM, Hu SY, Xu LN, Hong Y, Niyazi M, Gao XH, Ju LR, Zhang LQ, Feng XX, et al.. A multi-center survey of age of sexual debut and sexual behavior in Chinese women: suggestions for optimal age of human papillomavirus vaccination in China. Cancer Epidemiol. 2012;36:384–90. doi: 10.1016/j.canep.2012.01.009. PMID:22377277 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Chow SN, Soon R, Park JS, Pancharoen C, Qiao YL, Basu P, Ngan HY. Knowledge, attitudes, and communication around human papillomavirus (HPV) vaccination amongst urban Asian mothers and physicians. Vaccine. 2010;28:3809–17. doi: 10.1016/j.vaccine.2010.03.027. PMID:20347631 [DOI] [PubMed] [Google Scholar]
- 19.Davis K, Dickman ED, Ferris D, Dias JK. Human papillomavirus vaccine acceptability among parents of 10- to 15-year-old adolescents. J Low Genit Tract Dis. 2004;8:188–94. doi: 10.1097/01.ogx.0000143866.29509.50 doi:. PMID:15874862 [DOI] [PubMed] [Google Scholar]
- 20.Bianco A, Pileggi C, Iozzo F, Nobile CG, Pavia M. Vaccination against human papilloma virus infection in male adolescents: knowledge, attitudes, and acceptability among parents in Italy. Hum Vaccin Immunother. 2014;10:2536–42. doi: 10.4161/21645515.2014.969614. PMID:25483471 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Wang W, Ma Y, Wang X, Zou H, Zhao F, Wang S, Zhang S, Zhao Y, Marley G, Ma W. Acceptability of human papillomavirus vaccine among parents of junior middle school students in Jinan, China. Vaccine. 2015;33:2570–6. doi: 10.1016/j.vaccine.2015.04.010. PMID:25887088 [DOI] [PubMed] [Google Scholar]
- 22.Zou H, Wang W, Ma Y, Wang Y, Zhao F, Wang S, Zhang S, Ma W. How university students view human papillomavirus (HPV) vaccination: A cross-sectional study in Jinan, China. Hum Vaccin Immunother. 2016;12:39–46. doi: 10.1080/21645515.2015.1072667. PMID:26308701 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23.Zhang Y, Wang Y, Liu L, Fan Y, Liu Z, Wang Y, Nie S. Awareness and knowledge about human papillomavirus vaccination and its acceptance in China: a meta-analysis of 58 observational studies. BMC Public Health. 2016;16:216. doi: 10.1186/s12889-016-2873-8. PMID:26936076 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.Zhang SK, Pan XF, Wang SM, Yang CX, Gao XH, Wang ZZ, Li M, Ren ZF, Zheng QQ, Ma W, et al.. Knowledge of human papillomavirus vaccination and related factors among parents of young adolescents: a nationwide survey in China. Ann Epidemiol. 2015;25:231–5. doi: 10.1016/j.annepidem.2014.12.009. PMID:25656922 [DOI] [PubMed] [Google Scholar]
- 25.Ozyer S, Uzunlar O, Ozler S, Kaymak O, Baser E, Gungor T, Mollamahmutoglu L. Awareness of Turkish female adolescents and young women about HPV and their attitudes towards HPV vaccination. Asian Pacific journal of cancer prevention: APJCP. 2013;14:4877–81. doi: 10.7314/APJCP.2013.14.8.4877. [DOI] [PubMed] [Google Scholar]
- 26.Schmeink CE, Gosens KC, Melchers WJ, Massuger LF, Bekkers RL. Young adults awareness of HPV and vaccine acceptance after introduction of the HPV vaccine in the Dutch national vaccination program. Eur J Gynaecol Oncol. 2011;32:481–6. PMID:22053657 [PubMed] [Google Scholar]
- 27.Navarro-Illana P, Diez-Domingo J, Navarro-Illana E, Tuells J, Aleman S, Puig-Barbera J “Knowledge and attitudes of Spanish adolescent girls towards human papillomavirus infection: where to intervene to improve vaccination coverage”. BMC Public Health. 2014;14:490. doi: 10.1186/1471-2458-14-490. PMID:24885391 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28.Alder S, Gustafsson S, Perinetti C, Mints M, Sundstrom K, Andersson S. Mothers' acceptance of human papillomavirus (HPV) vaccination for daughters in a country with a high prevalence of HPV. Oncol Rep. 2015;33:2521–8. doi: 10.3892/or.2015.3817. PMID:25738832 [DOI] [PubMed] [Google Scholar]
- 29.Al-Naggar RA, Bobryshev YV, Al-Jashamy K, Al-Musli M. Practice of HPV vaccine and associated factors among school girls in Melaka, Malaysia. Asian Pacific journal of cancer prevention: APJCP. 2012;13:3835–40. doi: 10.7314/APJCP.2012.13.8.3835. PMID:23098480 [DOI] [PubMed] [Google Scholar]
- 30.Blumenthal J, Frey MK, Worley MJ Jr., Tchabo NE, Soren K, Slomovitz BM. Adolescent Understanding and Acceptance of the HPV Vaccination in an Underserved Population in New York City. J Oncol. 2012;2012:904034. doi: 10.1155/2012/904034. PMID:22187557 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 31.Pandey D, Vanya V, Bhagat S, Vs B, Shetty J. Awareness and attitude towards human papillomavirus (HPV) vaccine among medical students in a premier medical school in India. PloS one. 2012;7:e40619. doi: 10.1371/journal.pone.0040619. PMID:22859950 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 32.Chelimo C, Wouldes TA, Cameron LD. Human papillomavirus (HPV) vaccine acceptance and perceived effectiveness, and HPV infection concern among young New Zealand university students. Sexual health. 2010;7:394–6. doi: 10.1071/SH10005. PMID:20719233 [DOI] [PubMed] [Google Scholar]
- 33.Bonafide KE, Vanable PA. Male human papillomavirus vaccine acceptance is enhanced by a brief intervention that emphasizes both male-specific vaccine benefits and altruistic motives. Sexually transmitted diseases. 2015;42:76–80. doi: 10.1097/OLQ.0000000000000226. PMID:25585065 [DOI] [PubMed] [Google Scholar]
- 34.Gao H, Okoror TA, Hyner GC. Focus Group Study of Chinese International Students' Knowledge and Beliefs About HPV Vaccination, Before and After Reading an Informational Pamphlet About Gardasil((R)). Journal of immigrant and minority health / Center for Minority Public Health. 2016;18:1085–92. doi: 10.1007/s10903-016-0349-7. [DOI] [PubMed] [Google Scholar]
- 35.Christian WJ, Christian A, Hopenhayn C. Acceptance of the HPV vaccine for adolescent girls: analysis of state-added questions from the BRFSS. The Journal of adolescent health: official publication of the Society for Adolescent Medicine. 2009;44:437–45. doi: 10.1016/j.jadohealth.2008.09.001. PMID:19380090. [DOI] [PubMed] [Google Scholar]
- 36.Lenselink CH, Schmeink CE, Melchers WJ, Massuger LF, Hendriks JC, van Hamont D, Bekkers RL. Young adults and acceptance of the human papillomavirus vaccine. Public Health. 2008;122:1295–301. doi: 10.1016/j.puhe.2008.02.010. PMID:18619631 [DOI] [PubMed] [Google Scholar]
- 37.Kwan TT, Tam KF, Lee PW, Chan KK, Ngan HY. The effect of school-based cervical cancer education on perceptions towards human papillomavirus vaccination among Hong Kong Chinese adolescent girls. Patient Educ Couns. 2011;84:118–22. doi: 10.1016/j.pec.2010.06.018. PMID:20650592 [DOI] [PubMed] [Google Scholar]
- 38.Chang IJ, Huang R, He W, Zhang SK, Wang SM, Zhao FH, Smith JS, Qiao YL. Effect of an educational intervention on HPV knowledge and vaccine attitudes among urban employed women and female undergraduate students in China: a cross-sectional study. BMC Public Health. 2013;13:916. doi: 10.1186/1471-2458-13-916. PMID:24088392. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 39.Zhang SK, Pan XF, Wang SM, Yang CX, Gao XH, Wang ZZ, Li M, Ren ZF, Zhao FH, Qiao YL. Perceptions and acceptability of HPV vaccination among parents of young adolescents: a multicenter national survey in China. Vaccine. 2013;31:3244–9. doi: 10.1016/j.vaccine.2013.05.046. PMID:23707446 [DOI] [PubMed] [Google Scholar]
- 40.Jaspers L, Budiningsih S, Wolterbeek R, Henderson FC, Peters AA. Parental acceptance of human papillomavirus (HPV) vaccination in Indonesia: a cross-sectional study. Vaccine. 2011;29:7785–93. doi: 10.1016/j.vaccine.2011.07.107. PMID:21821079 [DOI] [PubMed] [Google Scholar]
- 41.Oscarsson MG, Hannerfors AK, Tyden T. Young women's decision-making process for HPV vaccination. Sexual & reproductive healthcare: official journal of the Swedish Association of Midwives. 2012;3:141–6. doi: 10.1016/j.srhc.2012.10.002. [DOI] [PubMed] [Google Scholar]
- 42.Dinh TA, Rosenthal SL, Doan ED, Trang T, Pham VH, Tran BD, Tran VD, Phan GA, Chu HK, Breitkopf CR. Attitudes of mothers in Da Nang, Vietnam toward a human papillomavirus vaccine. The Journal of adolescent health: official publication of the Society for Adolescent Medicine. 2007;40:559–63. doi: 10.1016/j.jadohealth.2007.02.003. PMID:17531763 [DOI] [PubMed] [Google Scholar]
- 43.Harrell FE. Regression modeling strategies: with applications to linear models, logistic regression, and survival analysis. New York: Springer-Verlag. 2001. [Google Scholar]
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