Awareness regarding and vaccines acceptability of human papillomavirus among parents of middle school students in Zunyi, Southwest China

ABSTRACT

The objective of this study was to investigate the parent cognition of information regarding the human papillomavirus (HPV) and their willingness toward HPV vaccination of their middle-school-aged children in Zunyi, Guizhou Province, China.The results provide a basis for improving the awareness concerning HPV-related information as a key vaccination strategy for implementing the HPV vaccine in the local context. Methods include the random cluster sampling method and questionnaires to survey parents. General descriptive and single-factor analyses were used to assess cognition to determine factors influencing vaccine willingness. Of 1,074 parents, 28.2% (302) and 38.0% (408) had heard of HPV and its vaccine before the survey, and when given HPV-related information, 73.9% (794) parents were willing to vaccinate their children. Reasons why parents did or did not want the vaccination were surveyed, with lack of sufficient knowledge about HPV and its vaccine being the primary reason to refuse vaccination. Concerns about safety, effectiveness, and perceiving low risk are the biggest obstacle in promoting vaccination. When the price is <1000, most parents (56.1%) are willing to vaccinate their children; thus, cost is also one of the concerns. Therefore, strategies for improving public awareness regarding the risk of cervical cancer and confidence in vaccination must be considered by policymakers.If the national authority confirms that the vaccine is safe and effective, the vaccine should be included in the national immunization program to increase publicity, address safety concerns, and allow for price regulation.

KEYWORDS:

• Cervical cancer
• cervical cancer vaccine
• human papillomavirus
• HPV
• vaccination laws
• China

Introduction

Cervical cancer is the second most common tumor that threatens Chinese women, with persistent infection by high-risk human papillomavirus (HPV) identified as the pathogenic condition underlying its onset.¹ Vaccination of young women before HPV exposure is the best preventive measure to reduce the risk of cervical cancer and its far-reaching implications on the future of public health.² Currently, the preventive HPV vaccine has been implemented in >160 countries and regions, including the bivalent (type 16 and 18) HPV vaccine of GlaxoSmithKline and the tetravalent (type 6, 11, 16, and 18) and nine-valet (type 6, 11, 16, 18, 31, 33, 45, 52, and 58) HPV vaccines of Merck.^3–5

The combination of HPV vaccination and cervical cancer screening is likely the most effective strategy for reducing the burden of cervical cancer. As the first cancer that can be prevented by vaccination, cervical cancer can be controlled or even eliminated under the two-pronged measures of prevention and treatment. From 2016 to 2017, bivalent and tetravalent HPV vaccines were approved by the China Food and Drug Administration, and the bivalent HPV vaccine has been introduced into clinical practice. On April 23, 2018, the Center for Drug Evaluation of the State Food and Drug administration accepted the application of Merck Sharp & Dohme Corp. to market two nine-valent human papillomavirus vaccines (Saccharomyces cerevisiae). The nine-valent cervical cancer vaccine was approved by the beginning of June; mainland China administered the first vaccination at the Bo’ao Super Hospital in Hainan.⁶

Early HPV vaccination can effectively prevent related diseases. The World Health Organization (WHO) proposes administering the HPV vaccination in middle school students who have not had sex as the primary approach for the prevention of cervical cancer.⁷ In addition, the WHO hopes to strengthen the global effort to eliminate cervical cancer by increasing awareness regarding the HPV vaccine.⁸ Currently, the HPV vaccine in China belongs to the second class of voluntary vaccinations; therefore, it is difficult to include it in the national immunization program.⁶ Middle-school-age girls do not have a clear understanding of HPV; therefore, the decision of whether to receive the HPV vaccination is primarily made by parents.^9,10 In China, there are few studies (especially in remote areas) on HPV-related awareness among parents of middle school students and few on the impact of different risk factors of HPV and vaccine cognition on parents’ willingness to vaccinate their children.

However, owing to the lack of specificity of symptoms of early cervical cancer, a considerable number of parents have low awareness regarding cervical cancer prevention and related knowledge, which is more prominent in remote areas with backward culture and information. The incidence of cervical cancer is expected to significantly decrease with the development of human papillomavirus (HPV) vaccine as a primary preventive method for cervical cancer. Therefore, it is of great significance to popularize HPV-related science among people with less education in poor areas. For the poor areas of Zunyi City, there are several problems associated with HPV screening and vaccination, such as wide area, large population in poor areas, scattered distribution, great differences in language and culture, low economic level, low education level, and poor awareness regarding self-care. Improved awareness and initiative of HPV vaccination in parents for their children in remote areas and better cooperation with the popularization of HPV can comprehensively improve the early diagnosis and treatment of cervical cancer and reduce the mortality rate.

Therefore, this study used a cross-sectional epidemiological survey to evaluate parents of middle school students in Zunyi City to determine their level of awareness, acceptance, and willingness to pay the vaccination costs, which will provide a reference for the development strategies for the publicity and the formulation of an HPV preventive vaccination plan for remote areas in China.

Methods

Study population

Between June and July, 2018, a cross-sectional survey was conducted among parents of middle school students from four schools in Zunyi City, Guizhou province, Southwest China. The study was approved by the Ethical Review Committee of School of Public Health, Zunyi Medical University. Informed consent was obtained from each participant prior to our survey.

Questionnaire

Of the four schools, two are junior high schools and two are senior high schools, each school have three grades, each grade has eight classes, and each class has 50 students. Therefore, two classes per grade of each school were randomly selected to participate the study. The questionnaire was only sent to the selected class, and all the parents of students in that class were invited to fill in the questionnaire. Referring to the relevant literature, locally and abroad, a self-designed questionnaire was used in this study. It comprised questions on sociodemographic characteristics, general knowledge of HPV and the HPV vaccine, and willingness toward HPV vaccination.After getting permission from the schools, a research assistant who had been trained in collecting data contacted the teachers to schedule an appointment to provide information regarding the study and deliver the questionnaires. The investigator sent a sealed envelope including informed consent, instructions for filling in the form, and the questionnaire to the middle school students. After a comprehensive explanation, the students took the paperwork to their parents to fill in. After the parents signed the informed consent form, they filled in the questionnaire as required, and then put it in a sealed envelope, which was handed to the investigator by the students.

Statistical analysis

EPI data 3.1 was used to establish a database for data entry and proofreading. SPSS 21.0 software was used for analysis. Descriptive statistics are provided in the form of the number and percentage (%) for categorical variables. A Chi-square test was used to compare the differences in the willingness of parents to vaccinate their children with HPV vaccine in correlation with the other characteristics (e.g., awareness regarding HPV). Binary logistic regression was used to analyze the factors influencing parents’ willingness to vaccinate their children. A two-sided P-value of <0.05 was considered significant.

Results

Demographic characteristics of the subjects

A total of 1,200 questionnaires were distributed and 1,074 valid questionnaires were collected, with an effective rate of 89.5%. As shown in Tables 1, 73.6% of the participants were female and >90% were Han; nearly three quarters of the parents were aged 36–45 years.

Table 1. Demographic characteristics of study participants (N = 1074)

Characteristics	Number	Frequency (%)
Survey respondent
Mother	760	70.8
Father	273	25.4
Others	41	3.8
Ethnic groups
Han	983	91.5
other	91	8.5
Age (years)
≤35	120	11.2
36–40	393	36.6
41–45	414	38.6
≥46	147	13.7
Education
Illiteracy	7	0.7
Primary	162	15.1
Secondary	661	61.6
Tertiary	244	22.7
Occupation
Freelance	206	19.2
Peasant	172	16.0
Unemployed	122	11.4
Self-employed	148	13.8
Worker	99	9.2
Clerk	91	8.5
other	235	21.9
Monthly gross earnings of the family(RMB)
≤4000	426	39.7
4001–8000	409	38.1
8001–12000	153	14.3
≥12001	85	7.9
Have you/your wife received cervical smear/cervical cancer screening in the past three years?
Yes	263	24.5
No	809	75.5
Have you/your wife been vaccinated against cervical cancer?
Yes	57	5.3
No	1017	94.7

The educational background of parents was as follows: 7 (0.7%) were illiterate, 162 (15.1%) were primary graduates, 661 (61.6%) were secondary graduates, and 244 (23.5%) were tertiary graduates. Regarding the occupation status of the parents, 206 (19.2%) were freelancers, 172 (16.0%) were peasants, 122 (11.3%) were unemployed, 148 (13.8%) were self-employed, 99 (9.2%) were workers, 91 (8.5%) were clerks, and 235 (21.9%) had jobs. In 2018, there were 426 (39.0%) parents whose average monthly income was less than or equal to 4,000 yuan, 409 (38.1%) parents whose average monthly income was 4,001–8,000 yuan, 153 (14.2%) parents whose average monthly income was 8,001–12,000 yuan, and 85 (7.9%) parents whose average monthly income was greater than or equal to 12,000 yuan. Only 263 (24.5%) female parents received cervical smear examination/cervical cancer screening and vaccination. Of those who had received cervical cancer screening, only 57 (5.3%) had received a cervical cancer vaccine.

Parents’ cognition of HPV and the HPV vaccine as well as their willingness to vaccinate their children

Through the investigation of parents’ cognition regarding human papillomavirus and human papillomavirus vaccine, it was found that only 302 (28.2%) of 1,072 parents had heard of HPV before the survey and 408 (38.0%) had heard of HPV Furthermore, 23.5% of the parents who had heard of the HPV vaccine had learned about the HPV vaccine from a physician’s consultation, 8.8% through school education, 20.3% through talking with family and friends, 19.9% through public welfare events, and 461% through media communication (including radio, television, newspapers, magazines, and Internet) on HPV-related information (Table 2).

Table 2. Sources of HPV vaccination related knowledge (N = 408)

Sources	Frequency	%
Doctor’s recommendation or consultation	96	23.5
School	36	8.8
Introduction of family or friends	83	20.3
Social benefit programs	81	19.9
Media consultation (including radio, TV, newspapers, magazines, and Internet)	188	46.1

Parents’ willingness to vaccinate their children with HPV vaccine

Of the 1,074 parents, 794 (74.0%) had willingness toward HPV vaccination of their daughters. Of the parents who gave a reason for unwillingness to vaccinate their children with the HPV vaccine, the primary reason (~44.5%) was that the vaccine had not been widely implemented in China and they were worried about its safety. The reasons why parents did or did not want the vaccination were surveyed; lack of sufficient knowledge about HPV and its vaccine was the primary reason to refuse vaccination. Most parents (61.5%) believed that the best time for HPV vaccination was before their first sexual encounter, and the main reason for their willingness to vaccinate their children was that they hoped their daughters would benefit from it (~46.5%). If the cervical cancer vaccine was proven to be safe and effective, most parents (53.4% and 48.8%) were willing to vaccinate their children. Concerns about safety, effectiveness, and perceiving low risk are the biggest obstacles in promoting vaccination. However, most parents (56.1%) were only willing to pay <1,000 yuan for their child’s HPV vaccination; thus, cost is also one of the concerns (Table 3).

Table 3. Attitude toward HPV vaccination

Item	Frequency	%
Would you like your daughter vaccinated against HPV vaccine?
Yes	794	73.9
No	274	25.5
Why you don’t want your daughter vaccinated with this vaccine: (274)
The child is too young to think that the child is at no risk of cervical cancer	104	38.0
The vaccine has not been widely used	62	22.6
Worry about the safety of vaccines	122	44.5
Worry about the effectiveness of the vaccine	80	29.2
Suspected source of vaccine	61	22.3
Vaccines are expensive	34	12.4
Fear that vaccination will encourage early sexual activity	20	7.3
Worry about being considered sexually active after vaccination	19	6.9
It’s up to the child to decide for himself	65	23.7
other	12	4.4
Why would you like your daughter to be vaccinated?
Daughters can benefit from it	500	46.5
Worried about her daughter’s future cervical cancer	401	37.3
Worried about her daughter suffering from genital warts in the future	180	16.7
Worried about her daughter’s future HPV infection	318	29.6
Worried that her daughter has been infected with HPV	85	7.9
other	20	1.8
The main reason for their willingness to vaccinate their children
Centers for Disease Control and Prevention	547	50.9
Community Health Service Center/local clinic	34	3.1
Maternal and child health care hospital	265	24.6
Comprehensive hospital	161	14.9
school	33	3.0
Any public health institution	27	2.5
What do you think is the best time to vaccinate against cervical cancer?
Before the first sex	661	61.5
After the first sex	209	19.4
other	195	18.1
In which of the following situations would you consider vaccinating your daughter against cervical cancer?
Cervical cancer vaccination is organized by the school	326	30.3
It has been proved that cervical cancer vaccine can effectively prevent cervical cancer	525	48.8
The cervical cancer vaccine has been confirmed to be safe	574	53.4
The cervical cancer vaccine is free	211	19.6
Doctors recommend vaccination against cervical cancer	331	30.8
The teacher suggested vaccination against cervical cancer	53	4.9
Cervical cancer vaccine is included in the national immunization program	447	41.6
If the domestic HPV vaccine is on the market, the highest price you are willing to bear
≤1000	603	56.1
1001–1500	224	20.8
1501–2000	116	10.8
2001–2500	59	5.4
2501–3000	35	3.2
3001–3500	31	2.8

Univariate analysis of parents’ willingness toward HPV vaccination of their children

Univariate analysis showed that there were significant differences among the attributes of parents’ educational background (P = .019), income (P = .009), whether the mother had a cervical smear examination/cervical cancer screening (P = .000), whether the mother had received the cervical vaccine (P = .000), and whether the parents had heard of HPV and the HPV vaccine (P = .000) (Table 4). Thus, these factors were the primary factors influencing parents to vaccinate their children.

Table 4. Single-factor analysis of factors influencing parents’ willingness willingness toward HPV vaccination of their daughters

		Number	%	X^2	P
Parents	Mother	589	74.9	0.642	.423
	Father	203	72.5
Ethnic	Han	727	74.4	0	.999
	others	64	74.4
Age	≤35	84	70.0	1.951	.583
	36–40	294	75.6
	41–45	337	73.7
	≥46	77	77.0
Education	Primary school or below	117	69.2	9.92	.019
	Junior middle school	313	77.1
	Enior school	175	69.2
	Undergraduate	189	78.8
Job	Freelance	154	74.8	5.304	.916
	Peasant	125	72.7
	Unemployed	88	72.1
	Self-employed	114	77
	Worker	73	74.5
	Clerk	67	74.4
Income	≤4000	308	72.5	11.612	.009
	4001–8000	293	72.0
	8001–12000	119	78.8
	≥12001	73	88.0
			0.0
Cervical cancer screened	Yes	218	83.5	15.338	.000
	No	575	71.3
Inject HPV vaccine*	Yes	48	84.2	3.073	.080
	No	746	73.8
Heard HPV	Yes	247	82.1	12.873	.000
	No	547	71.4
Heard vaccination	Yes	334	82.5	22.578	.000
	No	460	69.4

*Inject HPV vaccine: the parent who has received HPV vaccination.

Discussion

HPV is a DNA virus that infects humans and animals and can cause the proliferation of squamous epithelium in human skin and mucosa.¹¹ Currently, >130 strains of HPV have been isolated. According to the location of invasive tissue, HPV can be classified as a low-risk skin type, high-risk skin type, low-risk mucosal type, and high-risk mucosal type.¹² Studies have shown that persistent HPV infection is the main cause of cervical cancer and precancerous lesions, and it is also one of the important reasons why preventive measures against cervical cancer should begin in younger ages. The HPV vaccine can effectively prevent HPV infection and reduce the incidence of cervical cancer.¹³ Adolescent women are the target population for administering the HPV vaccine. The WHO and the American Advisory Committee on vaccination recommend 9–26 years old as the target HPV vaccination population, particularly girls aged 9–13 years. Considering the route of transmission of HPV and that the age of initial sexual behavior of Chinese women is 17 years, middle school students are the best group to target for administering the HPV vaccination in China.^14,15 Previous studies have shown that middle school students largely depend on their parents for making decisions, and their parents have the final right to make the decision regarding HPV vaccination of their children. Therefore, increasing parents’ awareness level regarding the HPV vaccine will impact their willingness to vaccinate their children.¹⁰ Understanding the attitudes of middle school students’ parents’ attitude toward the HPV vaccine will lead to appropriate strategies and methods for promoting awareness of this vaccine.

Although cervical vaccines are approved in >100 countries worldwide, the incidence of HPV vaccination varies in different countries. HPV vaccinations have achieved significant protective effects in countries with higher immunization rates, for example, in Australia, the incidence of severe cervical cancer in women significantly reduced after implementation of the HPV vaccine in adolescents and young adults.¹⁶ However, the HPV vaccination has not been conducted on a large scale in China, particularly in China’s economically disadvantaged areas. Therefore, it is of great significance to understand the parents’ understanding and acceptance of HPV and vaccine-related knowledge in remote areas, such as Zunyi City, which can provide the basis for the government to implement strategies on effective health education and publicity about HPV and the HPV vaccine to further improve the vaccination rate of adolescent girls and reduce the occurrence of cervical cancer. This study investigated the parents of middle school children in the Zunyi area of Guizhou Province to determine their cognition of HPV and the HPV vaccine and their views on HPV vaccination of adolescent girls.

This study shows that only 24.5% of mothers had received a cervical smear test/cervical cancer screening, 5.3% of mothers received cervical cancer vaccine, and ~28.2% and ~38.0% of parents have discussed HPV and HPV vaccine respectively, which is significantly lower than the survey results for other economically developed regions in China (Hong Kong, Shanghai, Guangzhou, Wuhan, etc.).¹⁷ Parents who had knowledge on HPV mainly learn about relevant information through media consultation (including radio, TV, news, magazines, and the Internet, etc.), which indicates that strengthening multimedia publicity will help to improve public awareness.

Of the parents surveyed, 73.9% of parents were willing to vaccinate their daughters with HPV vaccine, which was higher than the percentage reported for Xiamen, China,¹⁰ but lower than that reported for countries that had already included the HPV vaccine in a national immunization program.¹⁸ In previous studies, HPV awareness, family income, and education level were correlated with the vaccination willingness of respondents.¹⁹ In this study, demographic characteristics, age, income, and other basic factors were not correlated with vaccination willingness. The results of multivariate analysis showed that of the parents who had heard of the HPV and HPV vaccine, mothers who had received cervical smear examination/cervical cancer screening and had received a cervical cancer vaccine were promoting factors for willingness to vaccinate their daughter. Approximately 46.5% of those mothers were willing to vaccinate their daughters because they hoped their daughters would benefit from it. Moreover, most parents think that the best time for girls to receive the HPV vaccine is before they have their first sexual encounter. If the mother has been vaccinated, it indicates that she will be more willing to vaccinate her daughter. Those who did not want to be vaccinated were mainly worried about the safety and effectiveness of the vaccine (approximately 44.5%) or they believed that their daughters were young and at a low risk, therefore did not need to be vaccinated (approximately 38.0%).Concerns about the safety and effectiveness of vaccines are the biggest obstacles in the promotion of vaccination, consistent with the findings of previous studies, local and abroad.^19,20 Currently, the vaccine has been proved to be safe and effective.²¹ A randomized, double-blind trial showed that the efficacy of tetravalent HPV vaccine in preventing HPV (16/18)-related cervical intraepithelial neoplasia was 98.0%.Therefore, policy makers should consider the development of an effective strategy for strengthening public confidence in the vaccination.

Considering the costs of the HPV vaccine, 56.1% of the parents could accept a price of <1,000 yuan. Currently, the price of an imported cervical cancer vaccine in the domestic market for three doses is approximately 1,740–2,460 yuan, which is higher than the price that most parents can afford. At present, in Suzhou, China, parents can settle vaccine expenses with a medical insurance account,²² which changed their vaccination intention even if they previously had no intention to vaccinate. The price of HPV vaccine affected parents’ acceptance of HPV vaccination, consistent with previous literature.^23,24 The price of vaccine is likely to become an obstacle in vaccination; therefore, reducing the price of vaccine would be conducive to widespread vaccination. The inclusion of available medical insurance into the scope of HPV vaccine expenses will help to improve the willingness of parents toward HPV vaccination of their children.

In conclusion, parents of middle school students in Zunyi City of Guizhou province exhibited a high willingness toward HPV vaccination of their daughters, but the vaccination rate is low at this stage. Therefore, more publicity should be promoted, and local governments should be encouraged to introduce an available medical insurance policy that would cover the HPV vaccination. The implementation of these strategies would transform the willingness of parents to vaccinate their children, which would increase vaccination rates and thus lower the transmission of HPV and reduce the occurrence of cervical cancer.

The limitations of this study include the fact that it’s a cross-sectional design, which prevents us from assessing the temporal relationship between HPV vaccination intentions and parental knowledge and awareness. Second, our sample was not representative of the general China population, recruitment was limited to one province. In addition, we could not obtain information from middle school children because their school boards considered them to be too young. On the contrary, the major strengths of the study are its large size, the availability of information from parents, and it is also one of the few studies on this topic in Southwest China, which is socioeconomically and geographically different from other regions of the country.

Disclosure of potential conflicts of interest

No potential conflicts of interest were disclosed.

Additional information

Funding

This work was supported by the Start-up Research Fund for Master of Zunyi Medical University [No.F-769].