Skip to main content
Human Vaccines & Immunotherapeutics logoLink to Human Vaccines & Immunotherapeutics
. 2015 Aug 26;12(1):39–46. doi: 10.1080/21645515.2015.1072667

How university students view human papillomavirus (HPV) vaccination: A cross-sectional study in Jinan, China

Huachun Zou 1,#,*, Wei Wang 2,#, Yuanyuan Ma 3, Yongjie Wang 4, Fanghui Zhao 5, Shaoming Wang 5, Shaokai Zhang 5, Wei Ma 2,*
PMCID: PMC4962712  PMID: 26308701

Abstract

The acceptability of HPV vaccination among university students in China is not well understood. Our study was of cross-sectional study design. We collected a questionnaire about socio-demographic characteristics, knowledge of, attitude toward and acceptability of HPV vaccination. A total of 351 students were included in data analyses, among whom 47.6% were males and 70.0% aged 19–21. Only 10.3% had previously heard of HPV and 5.4% HPV vaccine. Male and female students were equally likely to accept HPV vaccine (71.8 vs 69.4%, p = 0.634) and recommend it to sexual partners (73.1 vs 76.7%, p = 0.441). The great majority of students could only afford RMB 300 (USD 50) or less for HPV vaccination. HPV vaccination acceptance was associated with being in year-one (Adjusted odds ratio (AOR)  = 3.78, 95% confidence interval (CI): 2.12–6.75), being from a key university (AOR = 1.88, 95%CI: 1.07–3.31), having heard of HPV-related morbidities (AOR = 1.88, 95% CI: 1.05–3.35), being concerned about HPV-related morbidities (AOR = 2.23, 95% CI: 1.16–4.27) and believing the vaccine should be given before first sexual contact (AOR = 2.44, 95% CI: 1.38–4.29). Female students were more likely to anticipate a late uptake of HPV vaccination (p = 0.002). The relatively lower levels of HPV knowledge but higher levels of vaccine acceptance among undergraduates highlighted the need for education on the roles of sexual behaviors in HPV transmission.

Keywords: China, college students, HPV, Human papillomavirus, vaccination

Introduction

Human papillomavirus (HPV) can cause morbidities that affect both men and women. Studies had shown that HPV is associated with nearly 85% of anal cancers, 70% of cervical cancers, 40% of vulval cancers, 50% of penile cancers, 35% of oropharyngeal cancers and 90% of ano-genital warts.1,2 These morbidities combined lay significant health and economic burdens for the society. In China the prevalence of HPV is high in both women and men. A study with 78,355 women (median age 37, range 18–75) in Guangdong Province (May 2011 to November 2012) found the overall HPV infection prevalence to be 7.3%, with HPV 6, 11, 16 and 18 accounting for the majority of all detected HPV infection types.3 There had been no study on the incidence of HPV in the general female population in China. Another study with 1,286 men (mean age 43, range 25–65) in Henan Province (2007 to 2009) found that the prevalence and incidence of any HPV type, oncogenic, and nononcogenic HPV were 17.8%, 6.4%, 12.4%, and 14.6, 4.9, 10.8 per 1,000 person months, respectively.4 It is estimated that any HPV was prevalent among 66.3% of men who have sex with men (MSM) in China.5

The quadrivalent vaccine (Gardasil) covers HPV 6, 11, 16 and 18. It is efficacious in preventing many of the above mentioned morbidities in both men and women. For example, Gardasil was efficacious to prevent nearly 100% of cervical cancers among women aged 18–24,6 90% of genital lesions among heterosexual men aged 16–26,7 78% of ano-genital warts and 75% of anal intraepithelial neoplasia among MSM.8 Its safety was also warranted in above-mentioned populations.6-8 The cost-effectiveness of HPV vaccination among these populations have also been well documented.9-11 In China, good tolerability and cost-effectiveness of HPV vaccine has been reported among 9–15 years old males and 9–45 years old females.12

Both the World Health Organization (WHO) and the US Food and Drug Administration (FDA) recommends the HPV vaccine to be used among men and women aged 9 through 26.13,14 Despite of the availability of HPV vaccination programs in over 50 countries, this vaccine is still yet to be approved in China. China failed to adopt the vaccine largely because of its unprecedented high price ($360 (RMB2160) for a 3-dose series in the United States).15 Some rich people in Chinese traveled to Hong Kong, South Korea or Japan to get HPV vaccine.16 With the declining age at first sexual contact and the compromised condom use, young students in China are vulnerable to sexually transmitted infections, HPV included.17,18 A successful HPV vaccination depends on not only the efficacy of the vaccine, but to a large extend, the awareness of the virus and acceptance of the vaccine among target populations. Until now there has been only one study that reported on the acceptability of HPV vaccination among university students in China.19 In that study, carried out in 7 cities in China in 2011, 70% of undergraduates expressed an accepting attitude toward HPV vaccination. Female students were more positive about receiving a vaccine than male students (73.2% vs 68.3%, p = 0.001). To inform future HPV vaccination policies in China, our study aimed to explore the knowledge of HPV and attitude toward HPV vaccination among university students in the populous province of Shangdong, China.

Results

Participant characteristics

In January 2013, a total of 375 students were approached and 355 students participated in the survey (refusal rate = 5.33%). Four were excluded from analysis because they completed less than 70% of the questions. As a result questionnaires of 351 students (171 males and 180 females) were used for data analyses. Table 1 shows the characteristics of participants. Among the participants, 47.6% were males, 70.0% aged between 19 and 21, 92.6% Han ethnic, 50.4% in year one, 45.5% in liberal art disciplines, and 68.1% from a key national university. Male students were significantly more likely to support pre-marital sex than their female counterparts (21.5 vs 2.8%, p < 0.001). Similarly significantly more male students had had sexual experience compared to female students (13.2 vs 1.7%, p < 0.001). No significant difference was observed between year-one and year-3 students in supporting pre-marital sex (5.8 vs 8.8%, p = 0.278) and having had sexual experience (12.1 vs 11.2%, p = 0.151).

Table 1.

Demographic characteristic of college students

Characteristics Males (%) Females (%) Total (%) P
Age (year)       0.208
 16–18 17(10.2) 28(15.9) 45(13.1)  
 19–21 118(70.7) 122(69.3) 240(70.0)  
 22–25 32(19.2) 26(14.8) 58(16.9)  
Ethnicity       0.057
 Han 162(95.3) 161(89.9) 323(92.6)  
 Other 8(4.7) 18(10.1) 26(7.4)  
Grade       0.869
 First year 87(50.9) 90(50.0) 177(50.4)  
 Third year 84(49.1) 90(50.0) 174(49.6)  
Major       0.813
 Liberal art 78(46.2) 79(44.9) 157(45.5)  
 Science 91(53.8) 97(55.1) 188(54.5)  
Type of university       0.414
 Key university 120(70.2) 119(66.1) 239(68.1)  
 None key university 51(29.8) 61(33.9) 112(31.9)  
Attitude toward pre-marital sex       <0.001
 Pro 35(21.5) 5(2.8) 40(11.7)  
 Con 29(17.8) 77(42.8) 106(30.9)  
 Neutral 99(60.7) 68(54.4) 197(57.4)  
Had sexual experience       <0.001
 Yes 22(13.2) 3(1.7) 25(7.3)  
 No 145(86.8) 173(98.3) 318(92.7)  

Knowledge of HPV and HPV vaccination

As shown in Table 2, before this study, only 10.3% of the students had heard of HPV. Over two thirds (70.7%) had heard of cervical cancer, anal cancer or genital warts. As low as 5.4% of had heard of HPV vaccine. Despite of relatively lower level of concern about HPV-related cancers (3.9 vs 45.3%, p < 0.001), more male students had ever inquired about HPV vaccine (5.8 vs 1.7%, p = 0.038). The majority of male (78.8%) and female (78.9%) students thought HPV vaccine should be available to both males and females. Slightly more male students thought the vaccine should be given before first sexual contact (55.3% vs 46.0%, p = 0.071). Female students tended to report a later anticipated age to receive HPV vaccine compared to male students. Significantly less female students thought the vaccine should best be given before 12 years old (5.1 vs 13.5%, p < 0.001) and more female students thought the vaccine is best to be given at university age than male students did (45.8 vs 32.2%, p = 0.002).

Table 2.

Perception of HPV vaccination among college students in Jinan, China

Item Males (%) Females (%) Total (%) P
Ever heard of HPV       0.223
 Yes 21(12.3) 15(8.3) 36(10.3)  
 No 150(87.7) 165(91.7) 315(89.7)  
Ever heard of cervical cancer/anal cancer/penile cancer/genital warts       0.699
 Yes 119(69.6) 129(71.7) 248(70.7)  
 No 52(30.4) 51(28.3) 103(29.3)  
Concerned of cervical cancer/anal cancer/penile cancer/genital warts       <0.001
 Yes 57(3.9) 81(45.3) 138(39.8)  
 No 75(44.6) 42(23.5) 117(33.7)  
 Not sure 36(21.4) 56(31.3) 92(26.5)  
Ever heard of HPV vaccine       0.195
 Yes 12(7.0) 7(3.9) 19(5.4)  
 No 159(93.0) 173(96.1) 332(94.6)  
Prior consultation regarding HPV vaccine information       0.038
 Yes 10(5.8) 3(1.7) 13(3.7)  
 No 161(94.2) 177(98.3) 338(96.3)  
Population to be vaccinated against HPV       0.973
 Male 9(5.3) 10(5.6) 19(5.4)  
 Female 9(5.3) 11(6.1) 20(5.7)  
 Both 134(78.8) 142(78.9) 276(78.9)  
 Not sure 18(10.6) 17(9.4) 35(10.0)  
Best time for HPV vaccination       0.071
 Before first sexual intercourse 94(55.3) 81(46.0) 175(50.6)  
 After first sexual intercourse 10(5.9) 6(3.4) 16(4.6)  
 Not sure 66(38.8) 89(50.6) 155(44.8)  
Best period for school/university based HPV vaccination       0.002
 Elementary school 22(12.9) 7(3.9) 29(8.3)  
 Junior middle school 23(13.5) 16(8.9) 39(11.1)  
 High school 45(26.3) 37(20.7) 82(23.4)  
 University 55(32.2) 82(45.8) 137(39.1)  
 Not sure 26(15.2) 37(20.7) 63(18.0)  
Best age for HPV vaccination (year)       0.001
 Before 12 23(13.5) 9(5.1) 32(9.2)  
 13–15 19(11.2) 14(7.9) 33(9.5)  
 16–18 42(24.7) 31(17.4) 73(21.0)  
 19–21 39(22.9) 47(26.4) 86(24.7)  
 22–25 12(7.1) 34(19.1) 46(13.2)  
 Not sure 35(20.6) 43(24.2) 78(22.5)  

Acceptance of HPV vaccination

As shown in Table 3, the majority of male and female students were equally likely to accept HPV vaccine (71.8 vs 69.4%, p = 0.634) and recommend it to their sexual partners (73.1 vs 76.7%, p = 0.441). Prospective health benefit of the vaccine was the reason behind the high acceptance of the vaccine and vaccine safety issues would potentially prevent students from taking the vaccine. The great majority of students would be able to afford an HPV vaccine priced at RMB 300 (USD 50) or less, whether it is domestically made (84.5%) or imported (79.7%). Female students were more likely to purchase HPV vaccine at a slightly higher price. Over half (52.9%) of students thought the government should promote HPV vaccination because it could effectively prevent cervical cancer, anal cancer and genital warts. Nearly half (49.7%) of students thought the government should negotiate vaccine price with manufacturers and subsidize HPV vaccination programs in China.

Table 3.

Attitude toward HPV vaccination among college students in Jinan, China

Item Males (%) Females (%) Total (%) P
Willing to take HPV vaccination       0.634
 No 48(28.2) 55(30.6) 103(29.4)  
 Yes 122(71.8) 125(69.4) 247(70.6)  
Willing to recommend HPV vaccination to partner       0.441
 No 46(26.9) 42(23.3) 88(25.1)  
 Yes 125(73.1) 138(76.7) 263(74.9)  
Reasons for willing to take HPV vaccination (Multiple)        
 Vaccine benefits self 107(85.6) 95(68.8) 202(76.8) 0.001
 Vaccine benefits others 66(52.8) 62(44.9) 128(48.7) 0.202
 Concern of cancers/genital warts 52(41.6) 72(52.2) 124(47.1) 0.086
 Fear of being infected with HPV in future 59(47.2) 82(59.4) 141(53.6) 0.047
 Fear of having been infected with HPV 14(11.2) 12(8.7) 26(9.9) 0.497
Reasons for not willing to take HPV vaccination (Multiple)        
 Low risk for cancers/genital warts 16(36.4) 13(32.5) 29(34.5) 0.651
 Limited usage to date in China 19(43.2) 14(35.0) 33(39.3) 0.393
 Concern of vaccine safety 37(84.1) 33(82.5) 70(83.3) 0.663
 Concern of vaccine efficacy 15(34.1) 20(50.0) 35(41.7) 0.169
 Doubt of vaccine manufacturer 21(47.7) 19(47.5) 40(47.6) 0.898
 High price of vaccine 10(22.7) 1(2.5) 11(13.1) 0.005
Affordable price for imported HPV vaccine (RMB)       0.025
 Under 100 92(54.1) 67(37.2) 159(45.4)  
 100—300 52(30.6) 68(37.8) 120(34.3)  
 300—500 12(7.1) 23(12.8) 35(10.0)  
 500—1000 5(2.9) 9(5.0) 14(4.0)  
 Above 1000 9(5.3) 13(7.2) 22(6.3)  
Affordable price for domestic HPV vaccine (RMB)       0.107
 Under 100 95(55.9) 81(45.3) 176(50.4)  
 100—300 51(30.0) 68(38.0) 119(34.1)  
 300—500 6(3.5) 14(7.8) 20(5.7)  
 500—1000 6(3.5) 8(4.5) 14(4.0)  
 Above 1000 12(7.1) 8(4.5) 20(5.7)  
Attitude toward future HPV vaccination promoting in China(Multiple)        
 Vaccine can prevent cancers/genital warts 96(56.5) 88(49.4) 184(52.9) 0.174
 Government should subsidize HPV vaccination 85(50.0) 88(49.4) 173(49.7) 0.878
 The price is too high to afford 40(23.5) 32(18.0) 72(20.7) 0.193
 Long-term effect of vaccine should be evaluated 42(43.3) 55(30.9) 97(27.9) 0.209
 HPV vaccine may lead to severe promiscuity 6(3.5) 6(3.4) 12(3.4) 0.928

Notes: 1USD=6.2 RMB at time of study.

Factors associated with HPV vaccine uptake

As shown in Table 4, by multivariate logistic regression, year-one students were more likely to take HPV vaccine than year-3 students (Adjusted odds ratio (AOR) = 3.78, 95% CI: 2.12–6.75). Students who had heard of cervical cancer, anal cancer or genital warts were almost 2 times as likely to take the vaccine than those who had not (AOR = 1.88, 95% CI: 1.05–3.35). Students who were concerned about cervical cancer, anal cancer or genital warts were over 2 times as likely to take the vaccine than those who were not (AOR = 2.23, 95% CI: 1.16–4.27). Students who thought the vaccine should best be given before first sexual contact were more likely to take the vaccine than those who did not (AOR = 2.44, 95% CI: 1.38–4.29).

Table 4.

Factors associated with willingness to take HPV vaccination among college students in Jinan, China

  Willing to take HPV vaccination
Item n/N ORξ (95% CIζ) AORδ (95% CI) P
Grade*            
 Third year 107/173 1   1    
 First year 140/177 2.33 1.45–3.75 3.78 2.12–6.75 <0.001
Major*            
 Liberal art 112/156 1   1    
 Science 130/188 0.88 0.55–1.40 0.68 0.38–1.21 0.19
Ethnicity*            
 Han 231/322 1   1    
 Other 16/26 0.63 0.28–1.44 0.46 0.17–1.24 0.12
Gender*            
 Male 122/170 1   1    
 Female 125/180 0.89 0.56–1.42 0.83 0.48–1.44 0.51
Type of university            
 None key university 70/112 1   1    
 Key university 177/238 1.74 1.08–2.82 1.88 1.07–3.31 0.03
Ever heard of cervical cancer/anal cancer/penile cancer/genital warts            
 No 60/103 1   1    
 Yes 187/247 2.23 1.37–3.64 1.88 1.05–3.35 0.03
Concern of cervical cancer/anal cancer/penile cancer/genital warts            
 No 71/117 1   1    
 Not sure 65/91 1.62 0.90–2.91 2.07 1.02–4.20 0.04
 Yes 107/138 2.24 1.30–3.86 2.23 1.16–4.27 0.01
Population to be vaccinated against HPV            
 Not sure 15/35 1        
 Male 14/19 0.26 0.12–0.53      
 Female 13/20 0.96 0.33–2.75      
 Both 205/275 0.63 0.24–1.65      
Best time for HPV vaccination            
 Not sure 94/154 1   1    
 Before first sexual intercourse 142/175 2.75 1.67–4.52 2.44 1.38–4.29 0.002
 After first sexual intercourse 9/16 0.82 0.29–2.32 1.52 0.37–6.29 0.56
Best age for HPV vaccination (year)            
 Not sure 42/75 1        
 Before 12 24/32 2.36 0.94–5.92      
 13–15 25/32 2.81 1.08–7.29      
 16–18 58/73 3.04 1.47–6.29      
 19–21 62/86 2.03 1.05–3.91      
 22–25 31/46 1.62 0.75–3.50      
Best period for school/university based HPV vaccination            
 Not sure 34/62 1        
 Elementary school 21/29 2.16 0.83–5.62      
 Junior middle school 31/39 3.19 1.27–8.04      
 High school 62/82 2.55 1.26–5.19      
 University 98/137 2.07 1.11–3.86      
Attitude toward pre-marital sex            
 Con 82/106 1        
 Pro 31/40 1.01 0.42–2.41      
 Neutral 130/196 0.58 0.34–0.99      

Notes:

*

Adjusted demographic characteristics.

ξ

OR, odds ratio (univariate logistic regression model).

δ

AOR, adjusted odds ratio (multivariable logistic regression model).

ζ

95%CI: 95% confidence interval.

Best age at HPV vaccination

As shown in Figure 1A, B, among male students 39.2% reported an age to take the vaccine that is equal to or higher than their age at first sexual contact or reported age. Among female students this figure was 47.2%. Female students were more likely to anticipate a late uptake of HPV vaccination (p = 0.002).

Figure 1.

Figure 1.

(A) Scatter plots of age when male students first had sex and age when male students would be willing to take HPV vaccination. Horizontal axis: age when male students first had sex. Vertical axis: age when male students would take HPV vaccination. Each hallow circle, rectangle and triangle represents an individual which could overlap. The diagonal dashed line is an artificial line that simulates the scenario when male students first had sex equals to age when they would take HPV vaccination. No one was less than 10 years old for first sex. (B) Scatter plots of age when female students first had sex and age when female students would be willing to take HPV vaccination. Horizontal axis: age when male students first had sex. Vertical axis: age when male students would take HPV vaccination. Each hallow circle, rectangle and triangle represents an individual which could overlap. The diagonal dashed line is an artificial line that simulates the scenario when female students first had sex equals to age when they would take HPV vaccination. No one was less than 10 years old for first sex.

Discussion

This is the first study to investigate knowledge of and attitudes toward HPV vaccination among undergraduate students in Shandong, China. Our survey found low levels of HPV related knowledge among these young men and women. However, their high acceptance of HPV was promising. The acceptability of HPV among our participants was identical to that among university students in another study conducted previously in China (70.6 vs 70.8%). Both studies found that year-one students were more likely to take HPV vaccine than year-3 students; and students who were concerned about cervical cancer, anal cancer or genital warts were over 2 times as likely to take the vaccine than those who were not. The other study also found students from key universities were more likely to take the vaccine (AOR = 1.30, 95% CI: 1.09–1.56).19 Studies in a number of countries had demonstrated that an extension of the current HPV program to include both boys and girls is a cost effective preventive intervention that would lead to a faster prevention of cancers, cancer precursors and genital warts in men and women.20-22 A high coverage in both genders will help achieve herd immunity and largely eradicate this virus.

In China, age of sexual debut has been decreasing in both men and women.23 HPV prevalence and cervical intraepithelial neoplasia (CIN) were high in young women in China. For example a study in Jiangsu Province found that among women aged 18 to 25, 17.1% were positive for HPV DNA and 3.4% had grade 2 or worse lesions of CIN.24 This study indicated cervical disease burden was relatively high among young women aged 18–25 and educational interventions targeting female adolescents and strategies to subsidize vaccine costs were needed to ensure the effectiveness of vaccination campaigns in China. Unfortunately until now the understanding of the natural history of HPV among young male populations in China is still lacking. Findings suggest that HPV vaccination of women between the ages of 13 and 15 years, before the completion of national compulsory education, is likely to contribute to the prevention of HPV infection and cervical cancer in China.23

Perceived susceptibility to HPV-related cancers contributed significantly to the acceptance of HPV vaccine among undergraduates in our study. This is consistent with findings from other countries in the pacific region.25 Very few undergraduates had ever heard of HPV and HPV vaccine. A great proportion of them did not know the best age to take the vaccine. This might be because they did not clearly understand the transmitting route of HPV. HPV-related knowledge and HPV vaccine acceptability can be improved by the incorporation of lecture-based education initiative into a government-sponsored or school-based program.26 HPV education should not only include the route of transmission and preventive measures, it should also include the efficacy and safety of HPV vaccination. This is because over 80% of undergraduates who would not take the vaccine refused HPV vaccination because of the concern of its safety.

An obstacle for HPV vaccination was its high price. Priced at USD450 it is the single most expensive vaccine. The majority of undergraduates were only willing/able to pay up to RMB 300 to purchase HPV vaccine. This gap could significantly hinder HPV vaccination, which has been seen in other countries. Despite its high efficacy in preventing associated morbidities, over 70% of boys aged 16–20 in Australia would not be willing to pay for the vaccine, however, nearly 90% of them would be willing to take it if it was free of charge.27 Moreover, 65% of American college students would take the vaccine only if it was free to them.28 The young men and women in our study expressed their expectation that the government would negotiate with HPV vaccine manufacturers to bring down its price so that most of them could afford. China is trialing its own HPV vaccine. With the availability of upcoming domestically manufactured HPV vaccine and government negotiation, the price is expected to decrease significantly. The full HPV vaccination usually involves 3 does. As vaccine price is a big barrier against successful vaccination, researchers have compared the efficacy of preventing HPV infection and HPV-related morbidities among people receiving 3 doses with that among people receiving 2 doses of HPV vaccine. These studies have shown that 2 doses was not inferior to 3 doses in preventing HPV infection and HPV-related morbidities.29 This may further contribute to an affordable vaccine price.

Undergraduates in this study generally indicated a late age to obtain HPV vaccination. About half of them would be potentially exposed to HPV infection when they first engage in unprotected intercourse or other risk sexual behaviors. This raises the question as to how effective vaccination among this young population would be in preventing HPV acquisition. Ideally vaccination should precede the onset of any sexual activity but the reality is that at present, universal HPV vaccine programs is not yet available in China.

The study explored the difference between the age at which college students first had sex and age when they would be willing to take HPV vaccination, the obstacles to HPV vaccination. Appropriate measures to address the obstacles explored may be valuable for future HPV vaccination policies and campaigns among college students in China. However, this study still has certain limitations. First, participants were from a non-random sample. Thus, the generalization of our results should be cautious. Second, the questionnaire was designed by our research team and validity and reliability were not tested before the research. Moreover, caution should be taken when interpreting the findings in our study owing to the cross-sectional nature that prevents us from making any statements regarding causality.

The relatively lower levels of HPV knowledge but higher levels of vaccine acceptance among undergraduates highlighted the need for education on the roles of sexual behaviors of males as well as females in HPV transmission. Future research should examine whether education interventions to change awareness and concern of personal HPV infection risk for both male and female university students have an impact on sexual behavior and HPV vaccine acceptability in young adult populations.

Materials and Methods

Study design and participants

We calculated sample size based on the following formula: n=(Zα/2)2p(1p)E2, in which Zα/2 is the 100(1 − α/2) percentile of the standard normal distribution, p is the estimated HPV acceptance rate in our sample, E is allowed margin of error.30 Previous study showed that HPV vaccine acceptability was about 70% in undergraduate students in China. With an estimated HPV vaccine acceptance rate of 70% at 95% confidence level, it needed a sample size of 323 to achieve a 5% margin of error for our survey. The Chinese Ministry of Education classifies the top 112 universities as “key universities” and other universities as “non-key universities.”31 In January 2013, a cross-sectional study with multi-stage non-randomized cluster sampling was conducted in Jinan, Shandong, China. First one key university and one non-key university based in Jinan were randomly selected. Then a lower grade was randomly chosen from grade one and 2, a higher grade from grade 3 and 4 respectively. Students from randomly selected classes of the 2 selected grades were invited to participate in the survey. This stratified sampling was adopted to achieve relatively similar sample sizes between lower grade students and students of a higher grade.

Data collection

A questionnaire was developed based on previous research.23,32 The questionnaire mainly consisted of questions about socio-demographic characteristics, knowledge of HPV, HPV vaccine, HPV-related diseases, and acceptability of and attitude toward HPV vaccination.

Investigators were trained before the formal investigation was performed. Participants were informed of the study objectives and survey content. Consenting participants were invited to complete a self-administered questionnaire. In order to avoid cross-contamination, participants were asked to keep a distance from each other for the duration of the survey. Information was recorded anonymously in order to encourage honest responses. 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.

Data analysis

Epidata 3.1 was used to double input the collected data, which was then analyzed using SAS 9.1.3 software. Simple statistics such as percentage points were used to describe the characteristics of participants, perception of HPV and HPV vaccine, acceptability of and attitudes toward HPV vaccination. Chi-square test was used to test the difference between subgroups. Analyses with a p value < 0.05 (2-tailed test) was considered statistically significant. Univariate logistic regression analysis was performed to evaluate associations of willingness to take HPV vaccination. Variables with a p value < 0.10 in the univariate analysis were further entered into the multivariate logistic regression model, where adjusted odds ratios (AOR) and their corresponding 95% confidence intervals were calculated. Stepwise logistic regression analysis was performed in multivariable logistic regression model, in which demographic characteristics (grade, major, ethnicity, gender) were adjusted.33 Scatter plots by STATA 13.0 were used to compare students' anticipated age at HPV vaccination to their age at first sexual contact. For those who had not had sexual experience, we presumed their age at first sexual contact to be their actual age at the time of recruitment.

Disclosure of Potential Conflicts of Interest

No potential conflicts of interest were disclosed.

Acknowledgments

We thank the 2 universities involved in this survey and the undergraduates who helped to complete the questionnaires. We are also grateful to the investigators.

Funding

This study was supported in part by the Investigator Initiated Studies Program of Merck and Co., Inc. [IISP# 40302]. The opinions expressed in this paper do not necessarily represent those of Merck and Co., Inc.

References

  • 1.Watson M, Saraiya M, Ahmed F, Cardinez CJ, Reichman ME, Weir HK, Richards TB. Using population-based cancer registry data to assess the burden of human papillomavirus-associated cancers in the United States: overview of methods. Cancer 2008; 113:2841-54; PMID:18980203; http://dx.doi.org/ 10.1002/cncr.23758 [DOI] [PubMed] [Google Scholar]
  • 2.Grulich AE, Jin F, Conway EL, Stein AN, Hocking J. Cancers attributable to human papillomavirus infection. Sex Health 2010; 7:244-52; PMID:20719211; http://dx.doi.org/ 10.1071/SH10020 [DOI] [PubMed] [Google Scholar]
  • 3.Jing L, Zhong X, Zhong Z, Huang W, Liu Y, Yang G, Zhang X, Zou J, Jing C, Wei X. Prevalence of human papillomavirus infection in Guangdong Province, China: a population-based survey of 78; 355 women. Sex Transm Dis 2014; 41:732-8; PMID:25581810; http://dx.doi.org/ 10.1097/OLQ.0000000000000201 [DOI] [PubMed] [Google Scholar]
  • 4.Liu M, He Z, Zhang C, Liu F, Liu Y, Li J, Xu Z, Wang Q, Hang D, Shen N, et al.. Prevalence, incidence, clearance, and associated factors of genital human papillomavirus infection among men: a population-based cohort study in rural China. Cancer Epidemiol Biomarkers Prev 2014; 23:2857-65; PMID:25217154; http://dx.doi.org/ 10.1158/1055-9965.EPI-14-0365 [DOI] [PubMed] [Google Scholar]
  • 5.Chow EP, Tucker JD, Wong FY, Nehl EJ, Wang Y, Zhuang X, Zhang L. Disparities and risks of sexually transmissible infections among men who have sex with men in China: a meta-analysis and data synthesis. PLoS One 2014; 9:e89959; PMID:24587152; http://dx.doi.org/ 10.1371/journal.pone.0089959 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 6.Garland SM, Hernandez-Avila M, Wheeler CM, Perez G, Harper DM, Leodolter S, Tang GW, Ferris DG, Steben M, Bryan J, et al.. Quadrivalent vaccine against human papillomavirus to prevent anogenital diseases. N Engl J Med 2007; 356:1928-43; PMID:17494926; http://dx.doi.org/ 10.1056/NEJMoa061760 [DOI] [PubMed] [Google Scholar]
  • 7.Giuliano AR, Palefsky JM, Goldstone S, Moreira ED Jr., Penny ME, Aranda C, Vardas E, Moi H, Jessen H, Hillman R, et al.. Efficacy of quadrivalent HPV vaccine against HPV Infection and disease in males. N Engl J Med 2011; 364:401-11; PMID:21288094; http://dx.doi.org/ 10.1056/NEJMoa0909537 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 8.Palefsky JM, Giuliano AR, Goldstone S, Moreira ED Jr., Aranda C, Jessen H, Hillman R, Ferris D, Coutlee F, Stoler MH, et al.. HPV vaccine against anal HPV infection and anal intraepithelial neoplasia. N Engl J Med 2011; 365:1576-85; PMID:22029979; http://dx.doi.org/ 10.1056/NEJMoa1010971 [DOI] [PubMed] [Google Scholar]
  • 9.Kim JJ. Targeted human papillomavirus vaccination of men who have sex with men in the USA: a cost-effectiveness modelling analysis. Lancet Infect Dis 2010; 10:845-52; PMID:21051295; http://dx.doi.org/ 10.1016/S1473-3099(10)70219-X [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 10.Vanagas G, Padaiga Z, Kurtinaitis J, Logminiene Z. Cost-effectiveness of 12- and 15-year-old girls' human papillomavirus 16/18 population-based vaccination programmes in Lithuania. Scand J Public Health 2010; 38:639-47; PMID:20639275; http://dx.doi.org/ 10.1177/1403494810377684 [DOI] [PubMed] [Google Scholar]
  • 11.Kim JJ, Goldie SJ. Cost effectiveness analysis of including boys in a human papillomavirus vaccination programme in the United States. BMJ 2009; 339:b3884; PMID:19815582; http://dx.doi.org/ 10.1136/bmj.b3884 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12.Li R, Li Y, Radley D, Liu Y, Huang T, Sings HL, Zhang L, Wang W, Zhong X, Saah AJ. Safety and immunogenicity of a vaccine targeting human papillomavirus types 6, 11, 16 and 18: a randomized, double-blind, placebo-controlled trial in Chinese males and females. Vaccine 2012; 30:4284-91; PMID:22433961; http://dx.doi.org/ 10.1016/j.vaccine.2012.02.079 [DOI] [PubMed] [Google Scholar]
  • 13.FDA licensure of quadrivalent human papillomavirus vaccine (HPV4, Gardasil) for use in males and guidance from the Advisory Committee on Immunization Practices (ACIP). MMWR Morb Mortal Wkly Rep 2010; 59:630-2; PMID:20508594 [PubMed] [Google Scholar]
  • 14.World Health Organisation WHO recommendations for routine immunization - summary tables, Table 1, February 24, 2014. Available at: http://www.who.int/immunization/policy/Immunization_routine_table1.pdf [Google Scholar]
  • 15.Zhang WJ, Li F, Wang YH, Simayi D, Saimaiti A, Zou XG, Xiong CL, Gong FL, Cao YG. The case for semi-mandatory HPV vaccination in China. Nat Biotechnol 2013; 31:590-1; PMID:23839139; http://dx.doi.org/ 10.1038/nbt.2631 [DOI] [PubMed] [Google Scholar]
  • 16.HPV vaccines among Chinese women still a long way off Available at: http://en.people.cn/90882/8339695.html. Verified on: June 6, 2015. [Google Scholar]
  • 17.Tabora N, Zelaya A, Bakkers J, Melchers WJ, Ferrera A. Chlamydia trachomatis and genital human papillomavirus infections in female university students in Honduras. Am J Trop Med Hyg 2005; 73:50-3; PMID:16014831 [PubMed] [Google Scholar]
  • 18.Vivancos R, Abubakar I, Hunter PR. Sex, drugs and sexually transmitted infections in British university students. Int J STD AIDS 2008; 19:370-7; PMID:18595873; http://dx.doi.org/ 10.1258/ijsa.2007.007176 [DOI] [PubMed] [Google Scholar]
  • 19.Wang SM, Zhang SK, Pan XF, Ren ZF, Yang CX, Wang ZZ, Gao XH, Li M, Zheng QQ, Ma W, et al.. Human papillomavirus vaccine awareness, acceptability, and decision-making factors among Chinese college students. Asian Pac J Cancer Prev 2014; 15:3239-45; PMID:24815477; http://dx.doi.org/ 10.7314/APJCP.2014.15.7.3239 [DOI] [PubMed] [Google Scholar]
  • 20.Burger EA, Sy S, Nygard M, Kristiansen IS, Kim JJ. Prevention of HPV-related cancers in Norway: cost-effectiveness of expanding the HPV vaccination program to include pre-adolescent boys. PLoS One 2014; 9:e89974; PMID:24651645; http://dx.doi.org/ 10.1371/journal.pone.0089974 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 21.Olsen J, Jorgensen TR. Revisiting the cost-effectiveness of universal HPV-vaccination in Denmark accounting for all potentially vaccine preventable HPV-related diseases in males and females. Cost Eff Resour Alloc 2015; 13:4; PMID:25694771; http://dx.doi.org/ 10.1186/s12962-015-0029-9 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 22.Elbasha EH, Dasbach EJ. Impact of vaccinating boys and men against HPV in the United States. Vaccine 2010; 28:6858-67; PMID:20713101; http://dx.doi.org/ 10.1016/j.vaccine.2010.08.030 [DOI] [PubMed] [Google Scholar]
  • 23.Zhao FH, Tiggelaar SM, Hu SY, Xu LN, Hong Y, Niyazi M, Gao XH, Ju LR, Zhang LQ, Feng XX, et al.. A multi-center survey of age of sexual debut and sexual behavior in Chinese women: suggestions for optimal age of human papillomavirus vaccination in China. Cancer Epidemiol 2012; 36:384-90; PMID:22377277; http://dx.doi.org/ 10.1016/j.canep.2012.01.009 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 24.Hu SY, Hong Y, Zhao FH, Lewkowitz AK, Chen F, Zhang WH, Pan QJ, Zhang X, Fei C, Li H, et al.. Prevalence of HPV Infection And Cervical Intraepithelial Neoplasia And Attitudes towards HPV Vaccination among Chinese Women Aged 18–25 in Jiangsu Province. Chin J Cancer Res 2011; 23:25-32; PMID:23467401; http://dx.doi.org/ 10.1007/s11670-011-0025-3 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 25.Juntasopeepun P, Suwan N, Phianmongkhol Y, Srisomboon J. Factors influencing acceptance of human papillomavirus vaccine among young female college students in Thailand. Int J Gynaecol Obstet 2012; 118:247-50; PMID:22727336; http://dx.doi.org/ 10.1016/j.ijgo.2012.04.015 [DOI] [PubMed] [Google Scholar]
  • 26.Chang IJ, Huang R, He W, Zhang SK, Wang SM, Zhao FH, Smith JS, Qiao YL. Effect of an educational intervention on HPV knowledge and vaccine attitudes among urban employed women and female undergraduate students in China: a cross-sectional study. BMC Public Health 2013; 13:916; PMID:24088392; http://dx.doi.org/ 10.1186/1471-2458-13-916 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 27.Zou H, Grulich AE, Cornall AM, Tabrizi SN, Garland SM, Prestage G, Bradshaw CS, Hocking JS, Morrow A, Fairley CK, et al.. How very young men who have sex with men view vaccination against human papillomavirus. Vaccine 2014; 32:3936-41; PMID:24852719; http://dx.doi.org/ 10.1016/j.vaccine.2014.05.043 [DOI] [PubMed] [Google Scholar]
  • 28.Jones M, Cook R. Intent to receive an HPV vaccine among university men and women and implications for vaccine administration. J Am Coll Health 2008; 57:23-32; PMID:18682342; http://dx.doi.org/ 10.3200/JACH.57.1.23-32 [DOI] [PubMed] [Google Scholar]
  • 29.Kuehn BM. Two doses of HPV vaccine may be sufficient. JAMA 2011; 306:1643; PMID:22009089; http://dx.doi.org/ 10.1001/jama.2011.1480 [DOI] [PubMed] [Google Scholar]
  • 30.Pennsylvania State University Estimating a Proportion for a Large Population. Available at: https://onlinecourses.science.psu.edu/stat414/node/212. Verified on: June 22, 2015. [Google Scholar]
  • 31.Global University Network for Innovation Building World-Class Universities in China: From the View of National Strategies. Available at: http://www.guninetwork.org/resources/he-articles/building-world-class-universities-in-china-from-the-view-of-national-strategie. Verified on: June 22, 2015. [Google Scholar]
  • 32.Li J, Li LK, Ma JF, Wei LH, Niyazi M, Li CQ, Xu AD, Wang JB, Liang H, Belinson J, 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; PMID:19135493; http://dx.doi.org/ 10.1016/j.vaccine.2008.12.020 [DOI] [PubMed] [Google Scholar]
  • 33.Harrell Frank E., Jr. (2001) “Regression modeling strategies: With applications to linear models, logistic regression, and survival analysis,” Springer-Verlag, New York. [Google Scholar]

Articles from Human Vaccines & Immunotherapeutics are provided here courtesy of Taylor & Francis

RESOURCES