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Acceptability of human papillomavirus vaccine among parents of junior middle school students in Jinan, China
Vaccine 33 (2015) 2570–2576
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Acceptability of human papillomavirus vaccine among parents of junior middle school students in Jinan, China Wei Wang a , Yuanyuan Ma b , Xia Wang c , Huachun Zou d , Fanghui Zhao e , Shaoming Wang e , Shaokai Zhang e , Yong Zhao f , Gifty Marley a , Wei Ma a,∗ a
Department of Epidemiology and Health Statistics, School of Public Health, Shandong University, Jinan, China School of Finance & Economics, Shandong Jiaotong University, Jinan, China c Zaozhuang Vocational College of Science and Technology, Zaozhuang, China d School of Public Health and Community Medicine, University of New South Wales, Sydney, Australia e Department of Epidemiology, Cancer Institute of Chinese Academy of Medical Sciences, Peking Union Medical College, Beijing, China f The Middle School Attached to Shandong University, Jinan, China b
a r t i c l e
i n f o
Article history: Received 9 October 2014 Received in revised form 19 March 2015 Accepted 2 April 2015 Available online 14 April 2015 Keywords: Acceptability Attitude Papillomavirus vaccines Cervical cancer Parents
a b s t r a c t Objective: To determine the level of awareness on human papillomavirus (HPV) vaccine and acceptance of HPV vaccination among parents of junior middle school students. Methods: A cross sectional survey employing cluster sampling was conducted in Jinan, Shandong Province of China in January of 2013. Results: A total of 400 parents of junior middle school students participated in the questionnaire survey, among whom 360 (90%) completed valid questionnaires. About 88 (22.63%) parents had ever heard of HPV. Only one in ten (10.2%) knew about HPV vaccine. Parents willing to accept HPV vaccination for children accounted for 40.8%. Factors associated willing to accept HPV vaccination for children among parents were: female parent (AOR: 0.38, 95%CI: 0.21–0.67), having ever heard of HPV vaccine (AOR: 2.38, 95%CI: 1.01–5.61), thinking HPV vaccination should commence before sexual debut(AOR: 2.16, 95%CI: 1.21–3.85), thinking HPV vaccination should commence before 12 years old (AOR: 2.76, 95%CI: 1.02–7.46) or 13–15 years old (AOR: 4.75, 95%CI: 1.79–12.61), concern about suffering from cervical cancer and/or genital warts (AOR: 2.43, 95%CI: 1.31–4.50). About 60% of parents were in favor of future HPV vaccination promoting in China believing that HPV vaccine could efficiently prevent cervical cancer, anal cancer or genital warts, 37.4% of parents with expectation of governmental subsidy and price regulation. Conclusion: Parental awareness level of HPV vaccine and willingness to accept HPV vaccination for children was low. However, the general attitude of many participants toward future promoting of HPV vaccination in China was encouraging, particularly if certain expectations were met. © 2015 Elsevier Ltd. All rights reserved.
1. Introduction Cervical cancer is the fourth most common cancer among women, with an estimated 528,000 new cases and 266,000 deaths worldwide in 2012 [1]. In China, the estimated new cases and deaths from cervical cancer in 2012 were 62,000 and 30,000, respectively, indicating a high burden of cervical cancer within the population. Over time, prophylactic human papillomavirus (HPV) vaccines had been developed and proven safe and effective in preventing cervical cancer and genital warts [2–4]. As at the end of 2013, HPV vaccines were available in 45 countries, most of which are developed countries [5]. However, there is no established
∗ Corresponding author. Tel.: +86 531 88382141; fax: +86 531 88382553. E-mail address: [email protected] (W. Ma). http://dx.doi.org/10.1016/j.vaccine.2015.04.010 0264-410X/© 2015 Elsevier Ltd. All rights reserved.
national program for HPV related disease prevention in mainland China where phase III clinical trials of prophylactic HPV vaccines are still ongoing [6]. Evidence of feasibility and acceptability among the Chinese population is required before the HPV vaccine can be licensed for public use in China. It is anticipated that peoples attitude toward HPV vaccine may have a great influence on its promotion hence lots of studies on parental attitude toward HPV vaccination for children have been conducted in many countries [7–9]. For example, a study in Sweden reported that 76% of parents were willing to vaccinate their children [10]. Ezeanochie et al. found that in Nigeria, mothers with good knowledge on HPV related diseases were significantly more willing to accept HPV vaccination of their daughters than those with poor knowledge [11]. In addition, differences in views on HPV vaccination were also reported among parents. Parents of female children were more willing to accept HPV vaccination than
W. Wang et al. / Vaccine 33 (2015) 2570–2576
parent of male children [12,13]. Study on immigrant Hispanic men reported more fathers were willing to vaccinate their adolescent sons than their daughters [14], and this finding was similar to results observed in a Honduras study [15]. However, a study conducted in US among low income women revealed that, women with only a daughter were more willing than those with a son to vaccinate their child [16]. In Chinese history, men were the primary decision-makers for the family unit. However, in modern days women also play a significant role in decision making on the health of their children. Taking cultural differences into account, parental attitude toward HPV vaccination for boys and girls in China could be different in comparison to findings from other countries. HPV vaccines have been proved to be efficient in preventing HPV infection both in men and women [2,3]. Therefore, the World Health Organization and the U. S. Centers for Disease Control and Prevention has recommended HPV vaccines for use in both young females and males before the onset of sexual activity [17–19]. In China most adolescents experience their first sexual activity from 16 years and above [20], this therefore makes teenagers 15 years and below the target populations for HPV vaccination. The age of junior middle school students in China range from 12 to 15 years and their parents’ attitude toward HPV vaccination may have a great impact on their children’s uptake of HPV vaccine [21]. Also in a Mexico study, mothers’ knowledge of and attitude toward HPV vaccine was found to be correlated with vaccination in children [22]. Despite the fact that some studies about perception and acceptability of HPV vaccination among female adults have been conducted in mainland China and Hong Kong [23–25], data on parental views concerning HPV vaccination for their junior middle school children is limited, especially the difference between mother and father’s views on HPV vaccination for children. Our study aimed to evaluate parental views on HPV vaccination for their junior-middle-school aged children and explore potential barriers to promoting of HPV vaccination in China in the future. 2. Materials and methods 2.1. Participants The study was conducted in a junior middle school in Jinan which was selected by convenience in January, 2013. Parents of grade two students were selected as the target group. Parents of children from six randomly selected classes were invited to participate in the survey. Out of a total 718 students in the ten classes for grade two, 400 parents representing 55.7% of the total parent population participated in the study. The survey was conducted during parents’ meetings in the school for convenient organization. 2.2. Data collection A pre-tested structured questionnaire developed based on previous research and expert opinions was used in the assessment [24,26]. The questionnaire collected information on participants’: socio-demographic characteristics; knowledge of and views on HPV and HPV vaccine prior to participation in this study; and attitude toward future HPV vaccination for children. Socio-demographic characteristics data included: age; gender; race; marital status; educational level; occupation; personal annual income; age and gender of child in this grade. Information on knowledge of and views on HPV and HPV vaccine before participation in this study among parents collected included: knowledge of HPV, HPV related diseases, and HPV vaccine; concerns about suffering from cervical cancer and/or genital warts; history of actively seeking out information on HPV vaccine; willingness to accept HPV vaccination for children; attitude toward premarital
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sex; perceptions of most appropriate stage, age and education stage for HPV vaccination in children; reasons against HPV vaccination. In terms of parental attitude toward future HPV vaccination when HPV vaccine is introduced into China mainland, participants were asked about affordable price for domestic HPV vaccine; appropriate venue for HPV vaccination; the condition for accepting HPV vaccination in children; attitude toward the promotion of future HPV vaccination in China. Parents were informed of the study objectives and procedure, and of voluntary participation. Willing participants who provided informed consent were assessed with self-administered questionnaires during supervised by trained research investigators. In order to avoid cross-contamination, participants were made to keep distance from each other for the duration of the survey. Questionnaire with uncompleted items >40% and/or logic errors was excluded. 2.3. Data analysis Epidata 3.1 was used to double input the collected data, which was then analyzed using SPSS 21.0 software. Frequency and Percentages were used to describe the characteristics of participants, knowledge of and views on HPV and HPV vaccine, as well as attitude toward future HPV vaccination. Chi-square test was used to assess the difference between subgroups, with analyses conducted separately by parent gender and child gender. P < 0.05 (two-tailed test) was considered statistically significant. Univariate logistic regression analysis was performed to evaluate predictors of willingness to accept child vaccination against HPV. Variables with a P value <0.10 in the univariate analysis were further entered into a multivariable Table 1 Demographic characteristic of parents of junior middle school students in Jinan, China. Characteristics
Frequency (Na )
Percent (%)
Age of parents Age of child
346 351
41.77 ± 3.33b 13.57 ± 0.57b
Gender of child Male Female
168 185
47.6 52.4
Gender of parents Male Female
172 188
47.8 52.2
Race Others Han
6 351
1.68 98.3
Marriage Others Married
7 352
1.95 98.05
Education ≤Junior middle school Senior middle school University/college ≥Master
16 75 219 48
4.47 20.94 61.17 13.41
Occupation Managerial and technical staff Commercial/service personnel Workers or farmers Healthcare providers/educators Others
197 35 25 76 24
55.18 9.80 7.00 21.29 6.72
Personal annual income (RMB) <10 thousands 10–30 thousands 30–50 thousands 50–100 thousands >100 thousands
23 59 143 92 32
6.59 16.91 40.97 26.36 9.17
a b
Numbers do not add up to 360 due to missing data. Mean ± standard deviation.
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logistic regression model, where adjusted odds ratios (AOR) and their corresponding 95% confidence intervals were calculated. Forward approach was performed in multivariable logistic regression model.
were Han Chinese (98.3%), 98.0% were married, and 74.5% had university/college education or higher. More than half of parents were managerial and technical staff, and about two in five parents had an annual personal income of 30,000–50,000 RMB (approx. 4880–8133 USD). Table 1 shows the characteristics of participants.
2.4. Ethical statement The study was approved by the Institutional Review Board of the Cancer Institute of Chinese Academy of Medical Sciences (CICAMS). Informed consent was obtained from each participant before the questionnaires were administered to them. 3. Results 3.1. Demographic characteristics Three hundred and sixty (90%) of the 400 questionnaires administered were valid for data analyses. Forty questionnaires were excluded because the participants completed less than 60% of the questions. Participants consisted of 172 fathers and 188 mothers. The mean age of parents was 41.77 (SD = 3.33), mean age of students was 13.57 (SD = 0.57) and female students accounted for 52.4% of the selected student population. The majority of parents
3.2. Knowledge of and views on HPV and HPV vaccine The results in the first paragraph are shown in Table 2. Of the total participants, only 22.6% had heard of HPV prior to the study. However, 84.8% knew of cervical cancer/anal cancer/genital warts. Significant statistical difference was observed between mothers and fathers in awareness of HPV and HPV related diseases. Only 10% of participants had heard of HPV vaccine and no significant statistical difference existed between mothers and fathers. Parents who had the history of actively seeking out information on HPV vaccine accounted for 3.98%. About forty percent of parents were willing to accept HPV vaccination for children, with fathers being more likely to accept children’s HPV vaccination than mothers. About the most appropriate stage for HPV vaccination, 68.8% parents were indecisive and 28.2% concurred it should be before first sexual intercourse. Also, 27.5% of participants considered junior middle school or lower to be the appropriate education
Table 2 Knowledge of and views on HPV and HPV vaccine among parents of junior middle school students in Jinan, China: by gender of parents. Characteristics
Male (%)
Female (%)
Total* (%)
P value
Have you ever heard of HPV before participation in this study? No Yes
145 (85.29) 25 (14.71)
132 (70.21) 56 (29.79)
277 (77.37) 81 (22.63)
<0.001
Have you ever heard of cervical cancer/anal cancer/genital warts before participation in this study? No Yes
41 (24.12) 129 (75.88)
13 (7.03) 172 (92.97)
54 (15.21) 301 (84.79)
<0.001
Have you ever heard of HPV vaccine before participation in this study? No Yes
154 (92.22) 13 (7.78)
163 (87.63) 23 (12.37)
317 (89.80) 36 (10.20)
0.156
Do you have the history of actively seeking out information on HPV vaccine? No Yes
165 (99.40) 1 (0.60)
173 (93.01) 13 (6.99)
338 (96.02) 14 (3.98)
0.002
78 (47.85) 85 (52.15)
127 (70.17) 54 (29.83)
205 (59.59) 139 (40.41)
<0.001
110 (68.75) 46 (28.75) 4 (2.5)
124 (68.89) 50 (27.78) 6 (3.33)
234 (68.82) 96 (28.24) 10 (2.94)
0.892
Do you think which education stage is most appropriate for HPV vaccination in children? Do not know Primary school Junior middle school Senior middle school University
45 (28.13) 20 (12.5) 36 (22.5) 37 (23.13) 22 (13.75)
50 (27.62) 11 (6.08) 27 (14.92) 35 (19.34) 58 (32.04)
95 (27.86) 31 (9.09) 63 (18.48) 72 (21.11) 80 (23.46)
<0.001
Do you think at which age (years) HPV vaccination should start in children? Do not know ≤12 13–15 16–18 ≥19
29 (18.35) 25 (15.82) 26 (16.46) 46 (29.11) 32 (20.25)
33 (18.13) 14 (7.69) 19 (10.44) 39 (21.43) 77 (42.31)
62 (18.24) 39 (11.47) 45 (13.24) 85 (25.0) 109 (32.06)
<0.001
What are your reasons against HPV vaccination in children? (Multiple) Children are too young to be at risk Limited use to date in China Doubt of the safety of vaccine Doubt of efficacy of vaccine Doubt of vaccine source High price of vaccine children should decide themselves Others
28 (36.8) 31 (40.8) 54 (71.1) 28 (36.8) 18 (23.7) 4 (5.3) 14 (18.4) 1 (1.3)
62 (50.0) 46 (37.4) 88 (71.0) 52 (41.9) 35 (28.2) 9 (7.3) 25 (20.2) 1 (0.8)
90 (45.0) 77 (38.7) 142 (71.0) 80 (40.0) 53 (26.5) 13 (6.5) 39 (19.5) 2 (1.0)
Do you willing to accept HPV vaccination for your children? No Yes Do you think which stage is the most appropriate for HPV vaccination for children? Do not know Before first sexual intercourse After first sexual intercourse
*
Numbers do not add up to 360 due to missing data.
0.069 0.633 0.990 0.475 0.480 0.795 0.763 1.00
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stage for HPV vaccination. Twenty five percent of parents believed the preferable age for HPV vaccination was 16 to 18 years, while 24.7% suggested ages ≤15 years and 32.1% for ages ≥19 years. For reasons against HPV vaccination in children, “Doubt of the safety of vaccine” recorded the highest frequency, followed by parents’ belief that children are too young to have the risk of cervical cancer. Other recorded concerns included, “Doubt of efficacy of vaccine”, and “Limited use of vaccines to date in China”. There was no statistically significant difference between parental views on HPV and HPV vaccine on gender of children. Details are in Table 3. 3.3. Attitude toward future HPV vaccination in children Majority of parents (71.1%) believed the most appropriate venue for HPV vaccination was Centers for Disease Prevention and Control, and 1.45% opted for schools as the preferred venue. For cost of vaccines, 40.1% believed less than 100 RMB would be the affordable price, 30.4% parents opted for 100–300 RMB, while only 4.8% were willing to pay more than 1000 RMB. If HPV vaccine is to be included in the expand plan immunization (EPI), 81.0% parents were willing to accept HPV vaccination for their children, and 30.8% would accept it if most of their children’s friends would be vaccinated as well. In addition, 23.3% parents expected the cost of HPV vaccination to be covered by National Medical Insurance. Most parents displayed positive attitude toward the idea of future HPV vaccination in China particularly if certain condition/expectation are met (Table 4). 3.4. Predictors of HPV vaccination acceptability in children Five variables were identified to be significantly associated with acceptability of HPV vaccination for children based on the
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multivariate logistic regression analysis. Parents having ever heard of HPV vaccine (AOR: 2.38, 95%CI: 1.01–5.61); concern about suffering from cervical cancer and/or genital warts (AOR: 2.43, 95%CI: 1.31–4.50); and mothers (AOR: 0.38, 95%CI: 0.21–0.67) were more likely to report that HPV vaccination for children was an acceptable option. Also, parents who believed vaccination should be before first sexual intercourse (AOR: 2.16, 95%CI: 1.21–3.85), and parents who selected age ranges ≤12 years (AOR: 2.76, 95%CI: 1.02–7.46) and 13–15 years (AOR: 4.75, 95%CI: 1.79–12.61) as the initial vaccination age were also likely to report an acceptable option of HPV vaccination for children in junior middle school (Table 5). 4. Discussion In the study, parents’ awareness on HPV, HPV vaccine and acceptability of HPV vaccination for children in Jinan, China was assessed. The results showed that parents had a high level of awareness of HPV related morbidities, such as cervical cancer, anal cancer and genital warts, but awareness level on HPV was low. A similar result was observed in an Indonesia study, where 66% of parents were aware of cervical cancer but only 16% had heard of HPV [8]. However, a study in Cameroon reported that more than 75% of parents had heard of HPV. Their high awareness rate for HPV knowledge correlated with impacts from intervention programs implemented there. Educational interventions have been demonstrated to effectively increase HPV knowledge and vaccination in America [27,28]. In addition, school-based education program has been found to have a positive impact on adolescent girls’ perceptions toward HPV vaccination and their willingness to be vaccinated in a Hong Kong study [29]. In China mainland, lecturebased education was also proved to be effective [30]. These findings have provided policy makers with possible means and methods
Table 3 Knowledge of and views on HPV and HPV vaccine among parents of junior middle school students in Jinan, China: by gender of children. Characteristics
Male (%)
Female (%)
Total* (%)
P value
Do you have the history of actively seeking out information on HPV vaccine? No Yes
162 (97.6) 4 (2.4)
169 (94.4) 10 (5.6)
331 (95.9) 14 (4.1)
0.135
98 (60.1) 65 (39.9)
102 (58.6) 72 (41.1)
200 (59.3) 137 (40.7)
0.779
111 (69.4) 45 (28.1) 4 (2.5)
119 (68.4) 49 (28.2) 6 (3.4)
230 (68.9) 94 (28.1) 10 (3.0)
0.876
Do you think which education stage is most appropriate for HPV vaccination in children? Do not know Primary school Junior middle school Senior middle school University
43 (26.7) 17 (10.6) 30 (18.6) 39 (24.2) 32 (19.9)
50 (28.7) 14 (8.0) 32 (18.4) 32 (18.4) 46 (26.4)
93 (27.8) 31 (9.3) 62 (18.5) 71 (21.2) 78 (23.3)
0.465
Do you think at which age (years) HPV vaccination should start in children? Do not know ≤12 13–15 16–18 ≥19
26 (16.3) 20 (12.5) 21 (13.1) 47 (29.4) 46 (28.8)
33 (19.1) 19 (11.0) 23 (13.3) 38 (22.0) 60 (34.7)
59 (17.7) 39 (11.7) 44 (13.2) 85 (25.5) 106 (31.8)
0.517
What are your reasons against HPV vaccination in children? (Multiple) Children are too young to be at risk Limited use to date in China Doubt of the safety of vaccine Doubt of efficacy of vaccine Doubt of vaccine source High price of vaccine Children should decide for themselves Others
41 (44.1) 42 (45.2) 63 (67.7) 42 (45.2) 29 (31.2) 7 (7.5) 20 (21.5) 1 (1.1)
47 (46.1) 33 (32.7) 75 (73.5) 37 (36.6) 23 (22.5) 6 (5.9) 18 (17.6) 1 (1.0)
88 (45.1) 75 (38.7) 138 (70.8) 79 (40.5) 52 (26.7) 13 (6.7) 38 (19.5) 2 (1.0)
0.780 0.074 0.375 0.207 0.173 0.646 0.497 1.000
Do you think which stage is the most appropriate for HPV vaccination for children? No Yes Which is the most appropriate stage for HPV vaccination for children? Do not know Before first sexual intercourse After first sexual intercourse
*
Numbers do not add up to 360 due to missing data.
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Table 4 Parental attitude toward future HPV vaccination for junior middle school students in Jinan, China. Items
Gender of parent Male (%)
Affordable price for domestic HPV vaccine (RMB) Under 100 100–300 300–500 500–1000 Above 1000
Total (%)
P value
Female (%)
70 (44.6) 36 (22.9) 27 (17.2) 13 (8.3) 11 (7.0)
63 (36.0) 65 (37.1) 28 (16.0) 14 (8.0) 5 (2.9)
133 (40.1) 101 (30.4) 55 (16.6) 27 (8.1) 16 (4.8)
0.04
Which venue is the most appropriate for HPV vaccination? Centers for Disease Control and Prevention Community health center Maternal and child care hospital General hospital School Any health care center Do not know
114 (69.5) 7 (4.3) 5 (3.0) 4 (2.4) 3 (1.8) 19 (11.6) 12 (7.3)
132 (72.5) 15 (8.2) 8 (4.4) 8 (4.4) 2 (1.1) 12 (6.6) 5 (2.7)
246 (71.1) 22 (6.4) 13 (3.8) 12 (3.5) 5 (1.4) 31 (9.0) 17 (4.9)
0.12
Under what condition will you consent to the vaccination for your child? (Multiple) Strong recommendation by healthcare providers Inclusion in the EPI* Coverage by the National Medical Insurance Family members have history of related diseases Strong recommendation by family members If most of children’s friends are vaccinated Price below 100 RMB
40 (26.0) 119 (77.3) 41 (26.6) 8 (5.2) 9 (5.8) 44 (5.8) 15 (9.7)
27 (15.3) 149 (84.2) 36 (20.3) 15 (8.5) 11 (6.2) 58 (6.2) 12 (6.8)
67 (20.2) 268 (81.0) 77 (23.3) 23 (6.9) 20 (6.0) 102 (30.8) 27 (8.2)
0.02 0.11 0.18 0.24 0.89 0.41 0.33
98 (63.2) 59 (38.1) 19 (12.3) 33 (21.3) 6 (3.9) 3 (1.9)
99 (56.9) 64 (36.8) 25 (14.4) 54 (31.0) 4 (2.3) 4 (2.3)
197 (59.9) 123 (37.4) 44 (13.4) 87 (26.4) 10 (3.0) 7 (2.1)
0.24 0.81 0.58 0.05 0.61 1.00
Attitude towards future HPV vaccination promoting in China (Multiple) Favor, believe in HPV vaccine could efficiently prevent cervical cancer/genital warts Favor, with expectation of governmental subsidy and price regulation Neutral, the price is too high to afford Neutral, further evaluation is needed for long-term effects and side effects of the vaccine Oppose, HPV vaccine may lead to severe promiscuity Others *
EPI: expanded program on immunization.
to improve the people’s knowledge on HPV, HPV vaccine and to increase the acceptability rate for HPV vaccination. In addition to the low awareness of HPV vaccine, the results also showed that parental acceptability of HPV vaccination for their children was low. Only about forty percent of parents were willing to accept HPV vaccination for their children, with fathers being the majority. In contrast, parental acceptability of HPV vaccine for children was about 80–88% in America [31,32]. This discrepancy could be explained by the low awareness level on HPV vaccine among our study sample, since we observed that the awareness on HPV vaccine is positively correlated with parental willingness to vaccinate their children. It was also noted that mothers were less likely to report that HPV vaccination for children was an acceptable option than fathers. Zhang et al. reported that mothers may care more about children’s health care [33]. And among members of our study sample, a higher proportion of mothers (50%) believed that children in junior middle school were too young to be at risk of contracting HPV. In terms of the initial age of HPV vaccination, more mothers (42.31%) than fathers (20.25%) thought it should be at least 19 years. The World Health Organization reported that HPV immunization programs are expected to achieve the largest effect from high coverage of young adolescent before sexual debut [19]. In our study, participants who concurred with the recommendation that the stage before first sexual intercourse is the appropriate stage for vaccination were more willing to vaccinate their children than the other parents, and accounted for only 28% of the sample size. In addition, less than one in four of parents believed HPV vaccination should start from ages below 15 years, also had higher acceptability of HPV vaccination in children. These results indicate that many parents don’t know the exact appropriate stage for child HPV vaccination and didn’t understand the importance of vaccinating their children before first sexual intercourse, especially mothers. To eliminate this barrier, more specific information about HPV and HPV vaccines should be provided to parents to enlighten them on
the subject, since it would contribute to a full understanding of the vaccine and help them make a rational decision on vaccination. Majority of participants believed the most appropriate venue for HPV vaccination was the center for disease prevention and control, which is one of the official institutions for vaccination and is also responsible for management and vaccination of EPI vaccines. However, other institutions such as community health centers, schools, and general hospitals could play an important role in delivering the related knowledge on HPV morbidities and HPV vaccines, since it has proven to be effective in previous studies [27,29]. The barriers to HPV vaccination that has been frequently described in literature are the concerns about safety, efficacy and source of HPV vaccine [9,34,35]. Similar results were also found in our study. Belief that children are too young to be at risk of HPV infections was the second most frequent reason given against HPV vaccination for children. As HPV vaccines have not yet been licensed in China mainland, the parental concern about its limited use currently is understandable. All the same, public health campaigns are necessary to reassure parents of the safety and efficacy of HPV vaccine and the great importance of HPV vaccination for children to promote HPV vaccination in the future. Slomovitz reported that parents would not consent to have their children aged 8–14 years being vaccinated, one of the reasons was the belief that male children would not directly benefit from the vaccine [36]. However, HPV vaccine has proven to be efficient in preventing HPV infection in both men and women [17,18]. In our sampled parents, no statistically significant difference was observed between parental acceptability of HPV vaccination for male and female children. They might hold the point that both boys and girls can benefit from HPV vaccination. In cost assessment, other studies have found that the cost of vaccination could also be a barrier to increasing vaccination uptake rate [37,38]. A national health interview survey in the United States among women aged 18–26 years reported that more than 76.4%
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Table 5 Factors associated with the acceptability of HPV vaccination for children among parents of junior middle school students in Jinan, China. Factor*
Willingness to accept HPV vaccination for children Event/total
OR
AOR (n = 318)
95%CI
P value
Gender of parents Male Female
85/163 54/181
1 0.39
1 0.38
0.21–0.67
0.001
Heard of HPV vaccine No Yes
120/309 19/34
1 1.99
1 2.38
1.01–5.61
0.047
Which is the most appropriate stage for HPV vaccination Do not know Before first sexual intercourse After first sexual intercourse
78/229 56/96 3/10
1 2.71 0.83
1 2.16 2.66
1.21–3.85 0.53–13.33
0.028 0.009 0.235
Believe the most appropriate stage for HPV vaccination in school Do not know primary school Junior middle school Senior high school university
26/94 19/29 41/62 31/72 20/78
1 4.97 5.11 1.98 0.90
At which age(years) should vaccination start Do not know ≤12 13–15 16–18 ≥19
16/62 23/37 33/44 35/83 28/108
1 4.72 8.63 2.10 1.01
1 2.76 4.75 1.41 0.83
1.02–7.46 1.79–12.61 0.64–3.10 0.38–1.81
0.045 0.002 0.391 0.634
Concerns about suffering from cervical cancer and/or genital warts No Do not know Yes
33/104 23/61 81/175
1 1.30 1.85
1 1.37 2.43
0.64–2.95 1.31–4.50
0.420 0.005
Attitude to premarital sex Oppose Didn’t think about it Neutral Favor
83/188 8/32 39/99 5/11
1 0.42 0.82 1.05
* 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.
participants preferred to receive HPV vaccination free or at a lower cost [39]. In our study, over seventy percent of parents were willing to pay 300 RMB or less for HPV vaccination, while only 12.9% of parent could afford if it costs more than 500 RMB. However, the price of HPV vaccine is currently estimated at US $360 (about 2000 RMB) in some countries [40]. Therefore, health policy makers and governments need to explore ways to overcome this barrier as much as possible if HPV vaccines are to be introduced into China in future. When asked about factors that will encourage them to vaccinate their children, most parents (81.0%) hoped HPV vaccine should be included into the EPI, while some parents hoped it should be covered by the National Medical Insurance (23.3%) or recommended by healthcare providers (20.0%). This could provide several possible measures to bridge the gap. In addition, recommendation from healthcare providers may also have a positive influence on parents’ decision making, which is consistent with a finding in a Vietnam study [41]. In respect to attitude toward promotion of future HPV vaccination in China, about 60% of parents hold positive views citing that HPV vaccines could efficiently prevent cervical cancer, anal cancer and genital warts. Also, 37.4% of parents were in favor of future HPV vaccination with expectation of governmental subsidy and price regulation. Therefore, more effort is still be required to promote future HPV vaccine uptake and use in China. 5. Limitations There were some limitations in this study. Such as, causal conclusions can’t be drawn from our finding due to the nature of the
cross sectional study method employed. Second, selection bias may exist owning to non-responders, and we could not follow-up on non-responders since anonymity was applied in the survey; Moreover, since participants were from a convenient sample, the sampled parents may not reflect the majority of parents in China, but they could reflect the population with similar demographic characteristics, or even the population in the city of Jinan to some degree. 6. Conclusions Our results indicated a low awareness on HPV and the vaccine among parents. Parental acceptability of HPV vaccination for their children was also low. There was no significant difference statistically between parental acceptability of HPV vaccination for male and female children. Also, there is a general positive attitude among participants toward future HPV vaccination in China if vaccine safety is assured and the cost is reasonable or subsidized by the government. Acknowledgements We thank the middle school involved in this survey and participants who helped to complete the questionnaires. Special thanks to Dr. Youlin Qiao from the Cancer institute of Chinese Academy of Medical Science (CICAMS) for providing expertise in the development of the study. This study was funded by Merck. The grant number: IISP# 40302. Merck did not participate in any part of the study from study design to approval of the manuscript, except for supporting fund for this project.
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[21] Hertweck SP, LaJoie AS, Pinto MD, Flamini L, Lynch T, Logsdon MC. Health care decision making by mothers for their adolescent daughters regarding the quadrivalent HPV vaccine. J Pediatr Adolesc Gynecol 2013;26:96–101. [22] Sanchez Anguiano LF, Lechuga Quinones AM, Milla Villeda RH, Lares Bayona EF. Knowledge and acceptance of vaccine against human papillomavirus among mothers of students from Durango City, Mexico. Ginecol Obstet Mex 2013;81:77–85. [23] Lee PW, Kwan TT, Tam KF, Chan KK, Young PM, Lo SS, et al. Beliefs about cervical cancer and human papillomavirus (HPV) and acceptability of HPV vaccination among Chinese women in Hong Kong. Prev Med 2007;45:130–4. [24] Li J, Li LK, Ma JF, Wei LH, Niyazi M, Li CQ, et al. Knowledge and attitudes about human papillomavirus (HPV) and HPV vaccines among women living in metropolitan and rural regions of China. Vaccine 2009;27:1210–5. [25] Kwan TT, Chan KK, Yip AM, Tam KF, Cheung AN, Young PM, et al. Barriers and facilitators to human papillomavirus vaccination among Chinese adolescent girls in Hong Kong: a qualitative-quantitative study. Sex Transm Infect 2008;84:227–32. [26] Zhao FH, Tiggelaar SM, Hu SY, Zhao N, Hong Y, Niyazi M, et al. A Multi-center survey of HPV knowledge and attitudes toward HPV vaccination among women, government officials, and medical personnel in China. Asian Pac J Cancer Prev 2012;13:2369–78. [27] Reiter PL, Stubbs B, Panozzo CA, Whitesell D, Brewer NT. HPV and HPV vaccine education intervention: effects on parents, healthcare staff, and school staff. Cancer Epidemiol Biomarkers Prev 2011;20:2354–61. [28] Hopfer S. Effects of a narrative HPV vaccination intervention aimed at reaching college women: a randomized controlled trial. Prev Sci 2012;13:173–82. [29] 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. [30] Chang IJ, Huang R, He W, Zhang SK, Wang SM, Zhao FH, et al. Effect of an educational intervention on HPV knowledge and vaccine attitudes among urban employed women and female undergraduate students in China: a crosssectional study. BMC Public Health 2013;13:916. [31] Lenselink CH, Gerrits MM, Melchers WJ, Massuger LF, van Hamont D, Bekkers RL. Parental acceptance of human papillomavirus vaccines. Eur J Obstet Gynecol Reprod Biol 2008;137:103–7. [32] Brabin L, Roberts SA, Farzaneh F, Kitchener HC. Future acceptance of adolescent human papillomavirus vaccination: a survey of parental attitudes. Vaccine 2006;24:3087–94. [33] Zhang SK, Pan XF, Wang SM, Yang CX, Gao XH, Wang ZZ, et al. Perceptions and acceptability of HPV vaccination among parents of young adolescents: a multicenter national survey in China. Vaccine 2013;31:3244–9. [34] Barnack JL, Reddy DM, Swain C. Predictors of parents’ willingness to vaccinate for human papillomavirus and physicians’ intentions to recommend the vaccine. Womens Health Issues 2010;20:28–34. [35] Gillespie L, Hicks CW, Santana M, Worley SE, Banas DA, Holmes S, et al. The acceptability of human papillomavirus vaccine among parents and guardians of newborn to 10-year-old children. J Pediatr Adolesc Gynecol 2011;24:66–70. [36] Slomovitz BM, Sun CC, Frumovitz M, Soliman PT, Schmeler KM, Pearson HC, et al. Are women ready for the HPV vaccine. Gynecol Oncol 2006;103:151–4. [37] Jaspan DM, Dunton CJ, Cook TL. Acceptance of human papillomavirus vaccine by gynecologists in an urban setting. J Low Genit Tract Dis 2008;12:118–21. [38] Donders GG, Bellen G, Declerq A, Berger J, Van Den Bosch T, Riphagen I, et al. Change in knowledge of women about cervix cancer, human papilloma virus (HPV) and HPV vaccination due to introduction of HPV vaccines. Eur J Obstet Gynecol Reprod Biol 2009;145:93–5. [39] Laz TH, Rahman M, Berenson AB. Human papillomavirus vaccine uptake among 18- to 26-year-old women in the United States: National Health Interview Survey, 2010. Cancer 2013;119:1386–92. [40] The L. Cheaper HPV vaccines needed. Lancet 2008;371:1638. [41] Dinh TA, Rosenthal SL, Doan ED, Trang T, Pham VH, Tran BD, et al. Attitudes of mothers in Da Nang, Vietnam toward a human papillomavirus vaccine. J Adolesc Health 2007;40:559–63.
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Acceptability of human papillomavirus vaccine among parents of junior middle school students in Jinan, China Wei Wang a , Yuanyuan Ma b , Xia Wang c , Huachun Zou d , Fanghui Zhao e , Shaoming Wang e , Shaokai Zhang e , Yong Zhao f , Gifty Marley a , Wei Ma a,∗ a
Department of Epidemiology and Health Statistics, School of Public Health, Shandong University, Jinan, China School of Finance & Economics, Shandong Jiaotong University, Jinan, China c Zaozhuang Vocational College of Science and Technology, Zaozhuang, China d School of Public Health and Community Medicine, University of New South Wales, Sydney, Australia e Department of Epidemiology, Cancer Institute of Chinese Academy of Medical Sciences, Peking Union Medical College, Beijing, China f The Middle School Attached to Shandong University, Jinan, China b
a r t i c l e
i n f o
Article history: Received 9 October 2014 Received in revised form 19 March 2015 Accepted 2 April 2015 Available online 14 April 2015 Keywords: Acceptability Attitude Papillomavirus vaccines Cervical cancer Parents
a b s t r a c t Objective: To determine the level of awareness on human papillomavirus (HPV) vaccine and acceptance of HPV vaccination among parents of junior middle school students. Methods: A cross sectional survey employing cluster sampling was conducted in Jinan, Shandong Province of China in January of 2013. Results: A total of 400 parents of junior middle school students participated in the questionnaire survey, among whom 360 (90%) completed valid questionnaires. About 88 (22.63%) parents had ever heard of HPV. Only one in ten (10.2%) knew about HPV vaccine. Parents willing to accept HPV vaccination for children accounted for 40.8%. Factors associated willing to accept HPV vaccination for children among parents were: female parent (AOR: 0.38, 95%CI: 0.21–0.67), having ever heard of HPV vaccine (AOR: 2.38, 95%CI: 1.01–5.61), thinking HPV vaccination should commence before sexual debut(AOR: 2.16, 95%CI: 1.21–3.85), thinking HPV vaccination should commence before 12 years old (AOR: 2.76, 95%CI: 1.02–7.46) or 13–15 years old (AOR: 4.75, 95%CI: 1.79–12.61), concern about suffering from cervical cancer and/or genital warts (AOR: 2.43, 95%CI: 1.31–4.50). About 60% of parents were in favor of future HPV vaccination promoting in China believing that HPV vaccine could efficiently prevent cervical cancer, anal cancer or genital warts, 37.4% of parents with expectation of governmental subsidy and price regulation. Conclusion: Parental awareness level of HPV vaccine and willingness to accept HPV vaccination for children was low. However, the general attitude of many participants toward future promoting of HPV vaccination in China was encouraging, particularly if certain expectations were met. © 2015 Elsevier Ltd. All rights reserved.
1. Introduction Cervical cancer is the fourth most common cancer among women, with an estimated 528,000 new cases and 266,000 deaths worldwide in 2012 [1]. In China, the estimated new cases and deaths from cervical cancer in 2012 were 62,000 and 30,000, respectively, indicating a high burden of cervical cancer within the population. Over time, prophylactic human papillomavirus (HPV) vaccines had been developed and proven safe and effective in preventing cervical cancer and genital warts [2–4]. As at the end of 2013, HPV vaccines were available in 45 countries, most of which are developed countries [5]. However, there is no established
∗ Corresponding author. Tel.: +86 531 88382141; fax: +86 531 88382553. E-mail address: [email protected] (W. Ma). http://dx.doi.org/10.1016/j.vaccine.2015.04.010 0264-410X/© 2015 Elsevier Ltd. All rights reserved.
national program for HPV related disease prevention in mainland China where phase III clinical trials of prophylactic HPV vaccines are still ongoing [6]. Evidence of feasibility and acceptability among the Chinese population is required before the HPV vaccine can be licensed for public use in China. It is anticipated that peoples attitude toward HPV vaccine may have a great influence on its promotion hence lots of studies on parental attitude toward HPV vaccination for children have been conducted in many countries [7–9]. For example, a study in Sweden reported that 76% of parents were willing to vaccinate their children [10]. Ezeanochie et al. found that in Nigeria, mothers with good knowledge on HPV related diseases were significantly more willing to accept HPV vaccination of their daughters than those with poor knowledge [11]. In addition, differences in views on HPV vaccination were also reported among parents. Parents of female children were more willing to accept HPV vaccination than
W. Wang et al. / Vaccine 33 (2015) 2570–2576
parent of male children [12,13]. Study on immigrant Hispanic men reported more fathers were willing to vaccinate their adolescent sons than their daughters [14], and this finding was similar to results observed in a Honduras study [15]. However, a study conducted in US among low income women revealed that, women with only a daughter were more willing than those with a son to vaccinate their child [16]. In Chinese history, men were the primary decision-makers for the family unit. However, in modern days women also play a significant role in decision making on the health of their children. Taking cultural differences into account, parental attitude toward HPV vaccination for boys and girls in China could be different in comparison to findings from other countries. HPV vaccines have been proved to be efficient in preventing HPV infection both in men and women [2,3]. Therefore, the World Health Organization and the U. S. Centers for Disease Control and Prevention has recommended HPV vaccines for use in both young females and males before the onset of sexual activity [17–19]. In China most adolescents experience their first sexual activity from 16 years and above [20], this therefore makes teenagers 15 years and below the target populations for HPV vaccination. The age of junior middle school students in China range from 12 to 15 years and their parents’ attitude toward HPV vaccination may have a great impact on their children’s uptake of HPV vaccine [21]. Also in a Mexico study, mothers’ knowledge of and attitude toward HPV vaccine was found to be correlated with vaccination in children [22]. Despite the fact that some studies about perception and acceptability of HPV vaccination among female adults have been conducted in mainland China and Hong Kong [23–25], data on parental views concerning HPV vaccination for their junior middle school children is limited, especially the difference between mother and father’s views on HPV vaccination for children. Our study aimed to evaluate parental views on HPV vaccination for their junior-middle-school aged children and explore potential barriers to promoting of HPV vaccination in China in the future. 2. Materials and methods 2.1. Participants The study was conducted in a junior middle school in Jinan which was selected by convenience in January, 2013. Parents of grade two students were selected as the target group. Parents of children from six randomly selected classes were invited to participate in the survey. Out of a total 718 students in the ten classes for grade two, 400 parents representing 55.7% of the total parent population participated in the study. The survey was conducted during parents’ meetings in the school for convenient organization. 2.2. Data collection A pre-tested structured questionnaire developed based on previous research and expert opinions was used in the assessment [24,26]. The questionnaire collected information on participants’: socio-demographic characteristics; knowledge of and views on HPV and HPV vaccine prior to participation in this study; and attitude toward future HPV vaccination for children. Socio-demographic characteristics data included: age; gender; race; marital status; educational level; occupation; personal annual income; age and gender of child in this grade. Information on knowledge of and views on HPV and HPV vaccine before participation in this study among parents collected included: knowledge of HPV, HPV related diseases, and HPV vaccine; concerns about suffering from cervical cancer and/or genital warts; history of actively seeking out information on HPV vaccine; willingness to accept HPV vaccination for children; attitude toward premarital
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sex; perceptions of most appropriate stage, age and education stage for HPV vaccination in children; reasons against HPV vaccination. In terms of parental attitude toward future HPV vaccination when HPV vaccine is introduced into China mainland, participants were asked about affordable price for domestic HPV vaccine; appropriate venue for HPV vaccination; the condition for accepting HPV vaccination in children; attitude toward the promotion of future HPV vaccination in China. Parents were informed of the study objectives and procedure, and of voluntary participation. Willing participants who provided informed consent were assessed with self-administered questionnaires during supervised by trained research investigators. In order to avoid cross-contamination, participants were made to keep distance from each other for the duration of the survey. Questionnaire with uncompleted items >40% and/or logic errors was excluded. 2.3. Data analysis Epidata 3.1 was used to double input the collected data, which was then analyzed using SPSS 21.0 software. Frequency and Percentages were used to describe the characteristics of participants, knowledge of and views on HPV and HPV vaccine, as well as attitude toward future HPV vaccination. Chi-square test was used to assess the difference between subgroups, with analyses conducted separately by parent gender and child gender. P < 0.05 (two-tailed test) was considered statistically significant. Univariate logistic regression analysis was performed to evaluate predictors of willingness to accept child vaccination against HPV. Variables with a P value <0.10 in the univariate analysis were further entered into a multivariable Table 1 Demographic characteristic of parents of junior middle school students in Jinan, China. Characteristics
Frequency (Na )
Percent (%)
Age of parents Age of child
346 351
41.77 ± 3.33b 13.57 ± 0.57b
Gender of child Male Female
168 185
47.6 52.4
Gender of parents Male Female
172 188
47.8 52.2
Race Others Han
6 351
1.68 98.3
Marriage Others Married
7 352
1.95 98.05
Education ≤Junior middle school Senior middle school University/college ≥Master
16 75 219 48
4.47 20.94 61.17 13.41
Occupation Managerial and technical staff Commercial/service personnel Workers or farmers Healthcare providers/educators Others
197 35 25 76 24
55.18 9.80 7.00 21.29 6.72
Personal annual income (RMB) <10 thousands 10–30 thousands 30–50 thousands 50–100 thousands >100 thousands
23 59 143 92 32
6.59 16.91 40.97 26.36 9.17
a b
Numbers do not add up to 360 due to missing data. Mean ± standard deviation.
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logistic regression model, where adjusted odds ratios (AOR) and their corresponding 95% confidence intervals were calculated. Forward approach was performed in multivariable logistic regression model.
were Han Chinese (98.3%), 98.0% were married, and 74.5% had university/college education or higher. More than half of parents were managerial and technical staff, and about two in five parents had an annual personal income of 30,000–50,000 RMB (approx. 4880–8133 USD). Table 1 shows the characteristics of participants.
2.4. Ethical statement The study was approved by the Institutional Review Board of the Cancer Institute of Chinese Academy of Medical Sciences (CICAMS). Informed consent was obtained from each participant before the questionnaires were administered to them. 3. Results 3.1. Demographic characteristics Three hundred and sixty (90%) of the 400 questionnaires administered were valid for data analyses. Forty questionnaires were excluded because the participants completed less than 60% of the questions. Participants consisted of 172 fathers and 188 mothers. The mean age of parents was 41.77 (SD = 3.33), mean age of students was 13.57 (SD = 0.57) and female students accounted for 52.4% of the selected student population. The majority of parents
3.2. Knowledge of and views on HPV and HPV vaccine The results in the first paragraph are shown in Table 2. Of the total participants, only 22.6% had heard of HPV prior to the study. However, 84.8% knew of cervical cancer/anal cancer/genital warts. Significant statistical difference was observed between mothers and fathers in awareness of HPV and HPV related diseases. Only 10% of participants had heard of HPV vaccine and no significant statistical difference existed between mothers and fathers. Parents who had the history of actively seeking out information on HPV vaccine accounted for 3.98%. About forty percent of parents were willing to accept HPV vaccination for children, with fathers being more likely to accept children’s HPV vaccination than mothers. About the most appropriate stage for HPV vaccination, 68.8% parents were indecisive and 28.2% concurred it should be before first sexual intercourse. Also, 27.5% of participants considered junior middle school or lower to be the appropriate education
Table 2 Knowledge of and views on HPV and HPV vaccine among parents of junior middle school students in Jinan, China: by gender of parents. Characteristics
Male (%)
Female (%)
Total* (%)
P value
Have you ever heard of HPV before participation in this study? No Yes
145 (85.29) 25 (14.71)
132 (70.21) 56 (29.79)
277 (77.37) 81 (22.63)
<0.001
Have you ever heard of cervical cancer/anal cancer/genital warts before participation in this study? No Yes
41 (24.12) 129 (75.88)
13 (7.03) 172 (92.97)
54 (15.21) 301 (84.79)
<0.001
Have you ever heard of HPV vaccine before participation in this study? No Yes
154 (92.22) 13 (7.78)
163 (87.63) 23 (12.37)
317 (89.80) 36 (10.20)
0.156
Do you have the history of actively seeking out information on HPV vaccine? No Yes
165 (99.40) 1 (0.60)
173 (93.01) 13 (6.99)
338 (96.02) 14 (3.98)
0.002
78 (47.85) 85 (52.15)
127 (70.17) 54 (29.83)
205 (59.59) 139 (40.41)
<0.001
110 (68.75) 46 (28.75) 4 (2.5)
124 (68.89) 50 (27.78) 6 (3.33)
234 (68.82) 96 (28.24) 10 (2.94)
0.892
Do you think which education stage is most appropriate for HPV vaccination in children? Do not know Primary school Junior middle school Senior middle school University
45 (28.13) 20 (12.5) 36 (22.5) 37 (23.13) 22 (13.75)
50 (27.62) 11 (6.08) 27 (14.92) 35 (19.34) 58 (32.04)
95 (27.86) 31 (9.09) 63 (18.48) 72 (21.11) 80 (23.46)
<0.001
Do you think at which age (years) HPV vaccination should start in children? Do not know ≤12 13–15 16–18 ≥19
29 (18.35) 25 (15.82) 26 (16.46) 46 (29.11) 32 (20.25)
33 (18.13) 14 (7.69) 19 (10.44) 39 (21.43) 77 (42.31)
62 (18.24) 39 (11.47) 45 (13.24) 85 (25.0) 109 (32.06)
<0.001
What are your reasons against HPV vaccination in children? (Multiple) Children are too young to be at risk Limited use to date in China Doubt of the safety of vaccine Doubt of efficacy of vaccine Doubt of vaccine source High price of vaccine children should decide themselves Others
28 (36.8) 31 (40.8) 54 (71.1) 28 (36.8) 18 (23.7) 4 (5.3) 14 (18.4) 1 (1.3)
62 (50.0) 46 (37.4) 88 (71.0) 52 (41.9) 35 (28.2) 9 (7.3) 25 (20.2) 1 (0.8)
90 (45.0) 77 (38.7) 142 (71.0) 80 (40.0) 53 (26.5) 13 (6.5) 39 (19.5) 2 (1.0)
Do you willing to accept HPV vaccination for your children? No Yes Do you think which stage is the most appropriate for HPV vaccination for children? Do not know Before first sexual intercourse After first sexual intercourse
*
Numbers do not add up to 360 due to missing data.
0.069 0.633 0.990 0.475 0.480 0.795 0.763 1.00
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stage for HPV vaccination. Twenty five percent of parents believed the preferable age for HPV vaccination was 16 to 18 years, while 24.7% suggested ages ≤15 years and 32.1% for ages ≥19 years. For reasons against HPV vaccination in children, “Doubt of the safety of vaccine” recorded the highest frequency, followed by parents’ belief that children are too young to have the risk of cervical cancer. Other recorded concerns included, “Doubt of efficacy of vaccine”, and “Limited use of vaccines to date in China”. There was no statistically significant difference between parental views on HPV and HPV vaccine on gender of children. Details are in Table 3. 3.3. Attitude toward future HPV vaccination in children Majority of parents (71.1%) believed the most appropriate venue for HPV vaccination was Centers for Disease Prevention and Control, and 1.45% opted for schools as the preferred venue. For cost of vaccines, 40.1% believed less than 100 RMB would be the affordable price, 30.4% parents opted for 100–300 RMB, while only 4.8% were willing to pay more than 1000 RMB. If HPV vaccine is to be included in the expand plan immunization (EPI), 81.0% parents were willing to accept HPV vaccination for their children, and 30.8% would accept it if most of their children’s friends would be vaccinated as well. In addition, 23.3% parents expected the cost of HPV vaccination to be covered by National Medical Insurance. Most parents displayed positive attitude toward the idea of future HPV vaccination in China particularly if certain condition/expectation are met (Table 4). 3.4. Predictors of HPV vaccination acceptability in children Five variables were identified to be significantly associated with acceptability of HPV vaccination for children based on the
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multivariate logistic regression analysis. Parents having ever heard of HPV vaccine (AOR: 2.38, 95%CI: 1.01–5.61); concern about suffering from cervical cancer and/or genital warts (AOR: 2.43, 95%CI: 1.31–4.50); and mothers (AOR: 0.38, 95%CI: 0.21–0.67) were more likely to report that HPV vaccination for children was an acceptable option. Also, parents who believed vaccination should be before first sexual intercourse (AOR: 2.16, 95%CI: 1.21–3.85), and parents who selected age ranges ≤12 years (AOR: 2.76, 95%CI: 1.02–7.46) and 13–15 years (AOR: 4.75, 95%CI: 1.79–12.61) as the initial vaccination age were also likely to report an acceptable option of HPV vaccination for children in junior middle school (Table 5). 4. Discussion In the study, parents’ awareness on HPV, HPV vaccine and acceptability of HPV vaccination for children in Jinan, China was assessed. The results showed that parents had a high level of awareness of HPV related morbidities, such as cervical cancer, anal cancer and genital warts, but awareness level on HPV was low. A similar result was observed in an Indonesia study, where 66% of parents were aware of cervical cancer but only 16% had heard of HPV [8]. However, a study in Cameroon reported that more than 75% of parents had heard of HPV. Their high awareness rate for HPV knowledge correlated with impacts from intervention programs implemented there. Educational interventions have been demonstrated to effectively increase HPV knowledge and vaccination in America [27,28]. In addition, school-based education program has been found to have a positive impact on adolescent girls’ perceptions toward HPV vaccination and their willingness to be vaccinated in a Hong Kong study [29]. In China mainland, lecturebased education was also proved to be effective [30]. These findings have provided policy makers with possible means and methods
Table 3 Knowledge of and views on HPV and HPV vaccine among parents of junior middle school students in Jinan, China: by gender of children. Characteristics
Male (%)
Female (%)
Total* (%)
P value
Do you have the history of actively seeking out information on HPV vaccine? No Yes
162 (97.6) 4 (2.4)
169 (94.4) 10 (5.6)
331 (95.9) 14 (4.1)
0.135
98 (60.1) 65 (39.9)
102 (58.6) 72 (41.1)
200 (59.3) 137 (40.7)
0.779
111 (69.4) 45 (28.1) 4 (2.5)
119 (68.4) 49 (28.2) 6 (3.4)
230 (68.9) 94 (28.1) 10 (3.0)
0.876
Do you think which education stage is most appropriate for HPV vaccination in children? Do not know Primary school Junior middle school Senior middle school University
43 (26.7) 17 (10.6) 30 (18.6) 39 (24.2) 32 (19.9)
50 (28.7) 14 (8.0) 32 (18.4) 32 (18.4) 46 (26.4)
93 (27.8) 31 (9.3) 62 (18.5) 71 (21.2) 78 (23.3)
0.465
Do you think at which age (years) HPV vaccination should start in children? Do not know ≤12 13–15 16–18 ≥19
26 (16.3) 20 (12.5) 21 (13.1) 47 (29.4) 46 (28.8)
33 (19.1) 19 (11.0) 23 (13.3) 38 (22.0) 60 (34.7)
59 (17.7) 39 (11.7) 44 (13.2) 85 (25.5) 106 (31.8)
0.517
What are your reasons against HPV vaccination in children? (Multiple) Children are too young to be at risk Limited use to date in China Doubt of the safety of vaccine Doubt of efficacy of vaccine Doubt of vaccine source High price of vaccine Children should decide for themselves Others
41 (44.1) 42 (45.2) 63 (67.7) 42 (45.2) 29 (31.2) 7 (7.5) 20 (21.5) 1 (1.1)
47 (46.1) 33 (32.7) 75 (73.5) 37 (36.6) 23 (22.5) 6 (5.9) 18 (17.6) 1 (1.0)
88 (45.1) 75 (38.7) 138 (70.8) 79 (40.5) 52 (26.7) 13 (6.7) 38 (19.5) 2 (1.0)
0.780 0.074 0.375 0.207 0.173 0.646 0.497 1.000
Do you think which stage is the most appropriate for HPV vaccination for children? No Yes Which is the most appropriate stage for HPV vaccination for children? Do not know Before first sexual intercourse After first sexual intercourse
*
Numbers do not add up to 360 due to missing data.
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Table 4 Parental attitude toward future HPV vaccination for junior middle school students in Jinan, China. Items
Gender of parent Male (%)
Affordable price for domestic HPV vaccine (RMB) Under 100 100–300 300–500 500–1000 Above 1000
Total (%)
P value
Female (%)
70 (44.6) 36 (22.9) 27 (17.2) 13 (8.3) 11 (7.0)
63 (36.0) 65 (37.1) 28 (16.0) 14 (8.0) 5 (2.9)
133 (40.1) 101 (30.4) 55 (16.6) 27 (8.1) 16 (4.8)
0.04
Which venue is the most appropriate for HPV vaccination? Centers for Disease Control and Prevention Community health center Maternal and child care hospital General hospital School Any health care center Do not know
114 (69.5) 7 (4.3) 5 (3.0) 4 (2.4) 3 (1.8) 19 (11.6) 12 (7.3)
132 (72.5) 15 (8.2) 8 (4.4) 8 (4.4) 2 (1.1) 12 (6.6) 5 (2.7)
246 (71.1) 22 (6.4) 13 (3.8) 12 (3.5) 5 (1.4) 31 (9.0) 17 (4.9)
0.12
Under what condition will you consent to the vaccination for your child? (Multiple) Strong recommendation by healthcare providers Inclusion in the EPI* Coverage by the National Medical Insurance Family members have history of related diseases Strong recommendation by family members If most of children’s friends are vaccinated Price below 100 RMB
40 (26.0) 119 (77.3) 41 (26.6) 8 (5.2) 9 (5.8) 44 (5.8) 15 (9.7)
27 (15.3) 149 (84.2) 36 (20.3) 15 (8.5) 11 (6.2) 58 (6.2) 12 (6.8)
67 (20.2) 268 (81.0) 77 (23.3) 23 (6.9) 20 (6.0) 102 (30.8) 27 (8.2)
0.02 0.11 0.18 0.24 0.89 0.41 0.33
98 (63.2) 59 (38.1) 19 (12.3) 33 (21.3) 6 (3.9) 3 (1.9)
99 (56.9) 64 (36.8) 25 (14.4) 54 (31.0) 4 (2.3) 4 (2.3)
197 (59.9) 123 (37.4) 44 (13.4) 87 (26.4) 10 (3.0) 7 (2.1)
0.24 0.81 0.58 0.05 0.61 1.00
Attitude towards future HPV vaccination promoting in China (Multiple) Favor, believe in HPV vaccine could efficiently prevent cervical cancer/genital warts Favor, with expectation of governmental subsidy and price regulation Neutral, the price is too high to afford Neutral, further evaluation is needed for long-term effects and side effects of the vaccine Oppose, HPV vaccine may lead to severe promiscuity Others *
EPI: expanded program on immunization.
to improve the people’s knowledge on HPV, HPV vaccine and to increase the acceptability rate for HPV vaccination. In addition to the low awareness of HPV vaccine, the results also showed that parental acceptability of HPV vaccination for their children was low. Only about forty percent of parents were willing to accept HPV vaccination for their children, with fathers being the majority. In contrast, parental acceptability of HPV vaccine for children was about 80–88% in America [31,32]. This discrepancy could be explained by the low awareness level on HPV vaccine among our study sample, since we observed that the awareness on HPV vaccine is positively correlated with parental willingness to vaccinate their children. It was also noted that mothers were less likely to report that HPV vaccination for children was an acceptable option than fathers. Zhang et al. reported that mothers may care more about children’s health care [33]. And among members of our study sample, a higher proportion of mothers (50%) believed that children in junior middle school were too young to be at risk of contracting HPV. In terms of the initial age of HPV vaccination, more mothers (42.31%) than fathers (20.25%) thought it should be at least 19 years. The World Health Organization reported that HPV immunization programs are expected to achieve the largest effect from high coverage of young adolescent before sexual debut [19]. In our study, participants who concurred with the recommendation that the stage before first sexual intercourse is the appropriate stage for vaccination were more willing to vaccinate their children than the other parents, and accounted for only 28% of the sample size. In addition, less than one in four of parents believed HPV vaccination should start from ages below 15 years, also had higher acceptability of HPV vaccination in children. These results indicate that many parents don’t know the exact appropriate stage for child HPV vaccination and didn’t understand the importance of vaccinating their children before first sexual intercourse, especially mothers. To eliminate this barrier, more specific information about HPV and HPV vaccines should be provided to parents to enlighten them on
the subject, since it would contribute to a full understanding of the vaccine and help them make a rational decision on vaccination. Majority of participants believed the most appropriate venue for HPV vaccination was the center for disease prevention and control, which is one of the official institutions for vaccination and is also responsible for management and vaccination of EPI vaccines. However, other institutions such as community health centers, schools, and general hospitals could play an important role in delivering the related knowledge on HPV morbidities and HPV vaccines, since it has proven to be effective in previous studies [27,29]. The barriers to HPV vaccination that has been frequently described in literature are the concerns about safety, efficacy and source of HPV vaccine [9,34,35]. Similar results were also found in our study. Belief that children are too young to be at risk of HPV infections was the second most frequent reason given against HPV vaccination for children. As HPV vaccines have not yet been licensed in China mainland, the parental concern about its limited use currently is understandable. All the same, public health campaigns are necessary to reassure parents of the safety and efficacy of HPV vaccine and the great importance of HPV vaccination for children to promote HPV vaccination in the future. Slomovitz reported that parents would not consent to have their children aged 8–14 years being vaccinated, one of the reasons was the belief that male children would not directly benefit from the vaccine [36]. However, HPV vaccine has proven to be efficient in preventing HPV infection in both men and women [17,18]. In our sampled parents, no statistically significant difference was observed between parental acceptability of HPV vaccination for male and female children. They might hold the point that both boys and girls can benefit from HPV vaccination. In cost assessment, other studies have found that the cost of vaccination could also be a barrier to increasing vaccination uptake rate [37,38]. A national health interview survey in the United States among women aged 18–26 years reported that more than 76.4%
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Table 5 Factors associated with the acceptability of HPV vaccination for children among parents of junior middle school students in Jinan, China. Factor*
Willingness to accept HPV vaccination for children Event/total
OR
AOR (n = 318)
95%CI
P value
Gender of parents Male Female
85/163 54/181
1 0.39
1 0.38
0.21–0.67
0.001
Heard of HPV vaccine No Yes
120/309 19/34
1 1.99
1 2.38
1.01–5.61
0.047
Which is the most appropriate stage for HPV vaccination Do not know Before first sexual intercourse After first sexual intercourse
78/229 56/96 3/10
1 2.71 0.83
1 2.16 2.66
1.21–3.85 0.53–13.33
0.028 0.009 0.235
Believe the most appropriate stage for HPV vaccination in school Do not know primary school Junior middle school Senior high school university
26/94 19/29 41/62 31/72 20/78
1 4.97 5.11 1.98 0.90
At which age(years) should vaccination start Do not know ≤12 13–15 16–18 ≥19
16/62 23/37 33/44 35/83 28/108
1 4.72 8.63 2.10 1.01
1 2.76 4.75 1.41 0.83
1.02–7.46 1.79–12.61 0.64–3.10 0.38–1.81
0.045 0.002 0.391 0.634
Concerns about suffering from cervical cancer and/or genital warts No Do not know Yes
33/104 23/61 81/175
1 1.30 1.85
1 1.37 2.43
0.64–2.95 1.31–4.50
0.420 0.005
Attitude to premarital sex Oppose Didn’t think about it Neutral Favor
83/188 8/32 39/99 5/11
1 0.42 0.82 1.05
* 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.
participants preferred to receive HPV vaccination free or at a lower cost [39]. In our study, over seventy percent of parents were willing to pay 300 RMB or less for HPV vaccination, while only 12.9% of parent could afford if it costs more than 500 RMB. However, the price of HPV vaccine is currently estimated at US $360 (about 2000 RMB) in some countries [40]. Therefore, health policy makers and governments need to explore ways to overcome this barrier as much as possible if HPV vaccines are to be introduced into China in future. When asked about factors that will encourage them to vaccinate their children, most parents (81.0%) hoped HPV vaccine should be included into the EPI, while some parents hoped it should be covered by the National Medical Insurance (23.3%) or recommended by healthcare providers (20.0%). This could provide several possible measures to bridge the gap. In addition, recommendation from healthcare providers may also have a positive influence on parents’ decision making, which is consistent with a finding in a Vietnam study [41]. In respect to attitude toward promotion of future HPV vaccination in China, about 60% of parents hold positive views citing that HPV vaccines could efficiently prevent cervical cancer, anal cancer and genital warts. Also, 37.4% of parents were in favor of future HPV vaccination with expectation of governmental subsidy and price regulation. Therefore, more effort is still be required to promote future HPV vaccine uptake and use in China. 5. Limitations There were some limitations in this study. Such as, causal conclusions can’t be drawn from our finding due to the nature of the
cross sectional study method employed. Second, selection bias may exist owning to non-responders, and we could not follow-up on non-responders since anonymity was applied in the survey; Moreover, since participants were from a convenient sample, the sampled parents may not reflect the majority of parents in China, but they could reflect the population with similar demographic characteristics, or even the population in the city of Jinan to some degree. 6. Conclusions Our results indicated a low awareness on HPV and the vaccine among parents. Parental acceptability of HPV vaccination for their children was also low. There was no significant difference statistically between parental acceptability of HPV vaccination for male and female children. Also, there is a general positive attitude among participants toward future HPV vaccination in China if vaccine safety is assured and the cost is reasonable or subsidized by the government. Acknowledgements We thank the middle school involved in this survey and participants who helped to complete the questionnaires. Special thanks to Dr. Youlin Qiao from the Cancer institute of Chinese Academy of Medical Science (CICAMS) for providing expertise in the development of the study. This study was funded by Merck. The grant number: IISP# 40302. Merck did not participate in any part of the study from study design to approval of the manuscript, except for supporting fund for this project.
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