Hsu, Yu-Yun PHD, RN*; Fetzer, Susan Jane PHD, RN†; Hsu, Keng-Fu PHD, MD‡; Chang, Yuan-Yuan BSN, RN§; Huang, Chih-Pyng BSN, RN¶; Chou, Cheng-Yang MD‡
Human papillomavirus (HPV) infection is the most common sexually transmitted disease (STD) occurring in 10% of women worldwide. Similar prevalence is founded in Taiwan (9.2%).1 In Taiwan, women between the ages of 21 and 30 have the highest prevalence rate of 29.6%.2 HPV infection occurs primarily in adolescents and young adults, with a cumulative prevalence rate up to 82% in sexually active youth.3 HPV 18 and 16, high-risk types, cause 70% to 75% of cervical cancer while HPV 6 and HPV 11, low-risk types, cause 90% of genital warts.4,5 In Taiwan, cervical cancer is the fifth leading cancer in women, with 1977 new cases of cervical cancer and 874 women dying of the disease in 2005.6
Two HPV vaccines have been approved and are available in most countries, including Taiwan. Although the HPV vaccine is effective in preventing high and low risk HPV infections,7–9 the intention to obtain the HPV vaccines depends on individual health beliefs. The Health Belief Model describes an individual’s health-related actions that are influenced by many factors.10 Individuals take actions to prevent a disease or condition when they perceive their health is under threat. The perception of threat includes the subjective perception of susceptibility and the severity of disease. Individuals weigh cost, benefits, and barriers to actions before taking preventive actions. Cues to action, such as recommendations from significant others or media, play an important role in urging people to take preventive measures against disease.10,11
Previous research has shown that the acceptability of HPV vaccination is high among adolescent women and adult women in Western societies.12–14 A study of US male and female college students in 2003 showed that 74% of the students would accept a vaccine for HPV and genital herpes.14 Research has found that a high perceived risk of HPV exposure or infection is significantly related to the acceptability of HPV vaccination.14,15
Research has been conducted in Western countries but little is known about the intention to obtain the HPV vaccine in Taiwan, even though Taiwan is one of the highest risk areas for cervical cancer in the world.16 The purpose of this study was to examine the attitudes toward HPV and the intention to obtain the HPV vaccine among college women in Taiwan. In addition, the study sought to identify variables that could predict the likelihood of obtaining the HPV vaccine.
Full-time female undergraduate students attending 5 universities in southern Taiwan were invited to participate in the study. The 5 universities included 1 public and 4 private schools. Three of the universities offered health-related majors (e.g., nursing), in addition liberal arts departments (e.g., Chinese, history, business management, foreign language). Two universities offered either health-related majors or liberal arts.
Approval to conduct the study was obtained from the Institutional Review Board and the university administrations. Information about the study was either distributed by handing out flyers or introduced by researchers in person on the campus. Class leaders notified the researchers of the number of students willing to participate. Research assistants distributed a cover letter and research packets to the subjects after class. Each packet contained the research questionnaire and a return envelop. A cover letter defined HPV as a sexual infection which was responsible for genital warts and cervical cancer. Further, a HPV vaccine had been developed and was available to prevent the infection. The adverse effects and the price of the HPV vaccine were also mentioned. Data were collected from October 2007 to April 2008.
An investigator developed self-administered questionnaire in Mandarin, the HPV Belief questionnaire (HPVB), was developed by the researchers based on the Health Belief Model.10,11 The 46-item HPVB includes demographic information, gynecologic history, awareness of HPV and the HPV vaccine, HPV health beliefs vaccination subscale, and the intention to obtain the vaccine. Three experts in HPV, 2 gynecologic physicians and 1 PhD nurse educator, reviewed the HPVB for content validity. The questionnaire was tested on 6 undergraduate students for clarity and ease of reading. Revisions were made based on content expert and pilot subjects’ recommendations.
Awareness of HPV and HPV Vaccine.
Two yes or no questions assess the awareness of HPV and the HPV vaccine: “Have you heard of HPV?” “Have you heard of the anti-cervical cancer vaccine (HPV vaccine)?” Based on their awareness, subjects were placed into 1 of 4 groups: Group A had an awareness of HPV and the vaccine; Group B had an awareness of HPV but not the vaccine; Group C had an awareness of the vaccine but not HPV; Group D had neither an awareness of HPV nor the vaccine.
The HPVB subscale measures attitude toward HPV vaccination. Seventeen items evaluate 7 areas of health belief: susceptibility of cervical cancer and HPV infection (2 items), disease severity (3 items), attributes of HPV (1 item), efficacy of vaccine (3 items), cost and availability (2 items), adverse effects of vaccine (3 items), and recommendations from others (3 items). Each item is rated on a 5-point Likert scale from 1 being strongly disagree to 5 being strongly agree. Cronbach’s α of internal reliability ranged from 0.36 (disease severity) to 0.76 (recommendations from others).
Intention to obtain HPV vaccine was assessed by asking subjects to answer the question “What is your likelihood of obtaining a HPV vaccine?” The item requests each subject respond by marking a 10-cm horizontal rating scale with 1 cm gradations. The left hand side of the line is anchored with the label “ no intention” (0 cm) while the right hand side is anchored with the label “strongest intention” (10 cm). The centimeter gradation closet the subject’s mark was recorded as intention to obtain the HPV vaccine. Respondents whose scores fell below the sample median are classified as low intention.
The data were analyzed using SPSS Version 15.0. One-way ANOVA was applied to determine any demographic differences among the 4 groups. Simple logistic regressions were performed to examine odds ratios and Wald test for each predictor, including demographic variables and HPVB health belief subscale. The final model was analyzed with forward stepwise logistic regression to predict vaccination intention.
The HPVB questionnaire was returned by 974 female undergraduate students. Six students indicated they had received the HPV vaccine and were excluded from the final analysis (vaccination rate = 0.6%). One hundred twenty-three (12.6%) omitted the HPV vaccination intention rating scale. Analysis of demographic characteristics of these non-responders (n = 123) when compared to responders (n = 845) indicated differences in age, class standing, personal history of gynecological visits, and sexual experience (P < 0.05). Nonresponders were younger, had a lower class rank, no history of gynecological visit, and no sexual experience. Therefore, the nonresponders were dropped from further analysis, with 845 undergraduate women remaining in the sample.
The mean age of the 845 undergraduate women was 20.6 (SD = 1.6) years and ranged from 17.1 to 36.2 years old. A small percent (n = 65, 7.7%) had a family history of gynecologic cancer while over a quarter (n = 244, 28.9%) had a personal history for gynecological visits. Only 22.4% (n = 189) of the women admitted any sexual experience. The mean age at first sexual experience was18.3 years (SD = 1.7, range = 14–25).
Awareness of HPV and the Vaccine
Fifty percent of the subjects had heard of HPV with slightly more having heard of the HPV vaccine (57.4%). Group A (awareness of HPV and vaccine) was the largest group, whereas Group C (awareness of HPV but not vaccine) was the smallest group (Table 1). The 4 groups differed on age, class rank, major area of study, and personal history of gynecological visit (P < 0.05). Group A was older, had a higher class rank, and was more likely to be in a health-related major. In addition, the students who were aware of HPV expressed intention to obtain the vaccine and were more likely to have had a visit to gynecologists.
Results showed that the median score of vaccination intention in the undergraduate women was 60, which was used as the cut off point to categorize low (0–59) and high (60–100) intention women. Of every 10 students, 6 (63.1%) reported a high intention to be vaccinated.
Predictors of Vaccine Intention
Results of simple logistic regression indicated that 4 demographic characteristics were significant determinants of intention to obtain HPV vaccination (Table 2): age (OR: 1.12, 95% CI: 1.02–1.23), family history of gynecologic cancer (OR: 2.05, 95% CI: 1.13–3.75), personal history of gynecological visit (OR: 1.39, 95% CI: 1.01–1.90), sexual experience (OR: 1.82, 95% CI: 1.26–2.63), and awareness of HPV and vaccine (OR: 1.75, 95% CI: 1.24–2.48). Older undergraduate women were more likely to have an intention to be vaccinated as well as those with family history of gynecological cancer or a personal history of gynecological visit. Subjects who described themselves as sexually experienced were more inclined to seek the HPV vaccine. Finally, subjects in Group A, who were aware of HPV and the vaccine, had a higher intention to obtain the vaccine.
Six variables of the health belief subscale significantly predicted vaccination intention except adverse effects (Table 2). The 6 variable were susceptibility (OR: 1.22, 95% CI: 1.08–1.38), disease severity (OR: 1.44, 95% CI: 1.31–1.57), efficacy (OR: 1.11, 95% CI: 1.03–1.20), cost and availability (OR: 0.90, 95% CI: 0.83–0.97), attributes of HPV (OR: 1.26, 95% CI: 1.11–1.43), and recommendations from others (OR: 1.31, 95% CI: 1.23–1.40). Women who believed they were more susceptible to contract HPV expressed a greater intention to be vaccinated. Undergraduate women who considered cervical cancer as a severe disease or the result of a sexual infection (attributes of HPV) were more likely to consider vaccination. If subjects believed in the efficacy of the HPV vaccine they were more likely to become vaccinated. External influences such as cost, availability of vaccine, and recommendations of others impacted vaccination intention. When the cost and availability of the vaccine were not perceived as barriers, there was a more positive intention toward the HPV vaccine. Subjects who indicated that they had received recommendations from others to endorse the vaccination were more likely to have a high intention.
Model of Vaccination Intention
Forward stepwise logistic regression was used to identify a model that predicted vaccination intention. The final model included 5 variables: recommendations from others, disease severity, vaccine cost and availability, awareness of HPV and the vaccine, and sexual experience (Table 3). Chi-square (χ2 = 134.44, df = 7, P < 0.001) indicated that the 5-variable model significantly distinguishes between high and low vaccination. The model explained 24% (Nagelkerke R2) of the total variation in vaccination intention among undergraduate women. The ability of the model to classify subjects was impressive, as 69% of the subjects were correctly classified as having a high or low intention to obtain the vaccine. The model correctly classified 85% of the subjects with high intention and 43% of the subjects with low intention.
Influences of Sexual Experience on Vaccination
The majority (n = 517, 61.2%) of women reported a lack of sexual experience. Among the undergraduate women without sexual experience, 38.1% (n = 197) reported an awareness of HPV and the vaccine. Thirty percent (n = 156) of the undergraduate women reported neither awareness of HPV nor the vaccine. Sixty percent (n = 309) of the subjects expressed a high intention to be vaccinated.
Simple logistic regression indicated that 1 demographic variable and 5 variables significantly predicted vaccination intention: awareness of HPV and the vaccine (OR: 1.63, 95% CI: 1.07–2.51), disease severity (OR: 1.48, 95% CI: 1.24–1.54), efficacy (OR: 1.13, 95% CI: 1.03–1.25), cost and availability (OR: 0.87, 95% CI: 0.80–0.96), and recommendations from others (OR: 1.26, 95% CI: 1.17–1.37) (Table 4). Intention to obtain the vaccine was more likely in sexually inexperienced undergraduate women who believed that cervical cancer was a significant disease, that the vaccine was efficacious, affordable and available, and they had received recommendations from others. It is no surprise that sexually inexperienced undergraduates who were aware of HPV and the vaccine were more likely to obtain the vaccination.
Using forward stepwise regression, a 3-variable model, which included disease severity, cost and availability, and recommendations from others significantly distinguished high and low vaccination intention (χ2 = 81.34, df = 3, P < 0.001). The model explained 20% (Nagelkerke R2) of the variance in vaccination intention (Table 5).
Over 60% of the undergraduate women in this study had a high vaccination intention which is lower than that reported in Western studies. Research on adolescent women from adolescent health centers and STD clinics in the United States indicated acceptability on HPV vaccine between 66% and 77%.13,14,17,18 The difference between the United States and Taiwan in vaccination intention may reflect cultural differences and social beliefs. Hoover and others found19 that US adolescents and adult women perceive that the HPV vaccine is a weapon against sexual transmitted diseases rather than cervical cancer. In Taiwan, the HPV vaccine has been marketed as an anticancer vaccine, but not a vaccine against STDs. Since cervical cancer is a major health threat for women between the ages of 40 and 50 in Taiwan, young women may ignore the effect of the HPV vaccine on STDs.
Despite the approval of the HPV vaccine in Taiwan since 2006, less than half of the undergraduate women who provided data for this study had heard of HPV with slightly more aware of the HPV vaccine. In the early 2000’s, only 23% to 37% of young women in the United States had heard of HPV,19–21 these data are similar to the current awareness in Taiwan. However, there has been a great deal of improvement in the awareness of HPV and the HPV vaccine in Western societies. A study about the awareness of HPV and the vaccine among American women in 2009 showed that 88.6% of the women aged 18 to 49 years had heard of HPV.22 One Australian study found that 73% of female respondents came from University Health Services had heard of HPV and 33% of the respondents had heard of the HPV vaccine.23
The 123 undergraduate students who did not answer the vaccine intention item and were dropped from the current study may have had difficultly answering the item. Without knowledge or awareness, the students would not be able to reply to the intention to obtain the vaccine item. Undergraduate women in Group D (neither aware of HPV nor the vaccine) were more likely to report a low intention. Limited knowledge and awareness may influence a woman’s intention to become vaccination. Undergraduate women with a history of gynecological visit reported a higher HPV vaccination intention than others. This finding is similar to finding of Fazekas et al24 in the United States that revealed a high intention of HPV vaccination was related to a history of cervical abnormality among African-American adolescents and adult women. In Taiwan, women may learn more information about the HPV vaccine from health care providers are seen in clinics. It has been shown that young women who have a history of gynecologic disease are likely to have high self-efficacy to obtain the HPV vaccine.18 Conversely, 1 study found that a history of STD was not a significant predictor for HPV vaccination intention among American college students.14
Sexual experience is also a significant factor affecting an individual’s vaccination intention. Although HPV vaccine is recommended for sexually inexperienced adolescents and young women, the findings among Taiwanese undergraduate women show that young women may not have an intention to obtain HPV vaccine until they are sexually active. One reason for this could be that young women may only become aware of STD when they are engaged in sexual activity. The awareness of STD may encourage the HPV vaccination intention for those women who are sexual active.
Undergraduate women with stronger beliefs of their susceptibility for cervical cancer, the disease severity, and the attributes of HPV infection were more likely to obtain the HPV vaccine. These results are similar to previous findings that have shown disease severity to be significant predictors of acceptability of HPV or STD vaccines among college students and young women.12–14,25 Higher perceived likelihood of cervical cancer and perceived disease severity translate into a higher intention of vaccination.
As expected, beliefs about the efficacy, cost, and adverse effects of the HPV vaccine influence undergraduate women’s intention of vaccination. Consistent with prior reports,14,26 efficacy and price are 2 chief considerations for the acceptability of HPV vaccine in young women. While the HPV vaccine has been demonstrated as efficacious against the HPV infection, the high price of the HPV vaccine is still a barrier to vaccination. A 3-dose HPV vaccine costing about US $400 in Taiwan is not covered by insurance and is not affordable for the typical Taiwanese undergraduate woman or her family.
Recommendations from significant others, such as parents, friends, and health care providers influence the college women’s decision to consider vaccination. It is reasonable that recommendations from others or normative beliefs contribute to vaccination intention. Previous research has also demonstrated that undergraduate women’s intention to obtain HPV or HIV vaccinations are influenced by their significant others.12,14,27 Kahn et al12 showed that health care providers, parents and partners are significant in the endorsement of the HPV vaccine among young women. However, in relation to the HPV vaccine, it is unclear as to which individuals have the greatest influence in Taiwan, an area requiring further research.
This is the first study to examine the HPV awareness and intention of sexually inexperienced undergraduate women. Because the HPV vaccine is recommended for women before their first sexual experience, it is concerned that the final model of sexually inexperienced women included 3 variables that were only able to predict 19% of the variance. Previous research showed that self-efficacy is an influence to vaccination intention in young women.18 The roles of self-efficacy in the vaccination intention require additional investigation.
Limitations of the study include the recruitment of a convenience sample from 5 universities. It is possible that the subjects who participated in the study had a high interest in HPV or HPV vaccine issues and the intention to obtain the vaccine may have been overestimated. Another limitation is that the findings of this study focus on college aged women. Thus, the results cannot be generalized to adolescent girls under 17 years old. Finally, the current study assessed the intention to accept a HPV vaccine at personal cost. The results of this study cannot be extended to women who have access to a cost-free HPV vaccine.
Future research should assess the individual contribution of recommendations from others on vaccination intention, including parents, peers, and mass media. Furthermore, the recommended ideal age for HPV vaccination for young women is 9 to 26 years who have not yet experienced intercourse.9 Given this, further research is needed using a younger sample of women.
Additional information about HPV, cervical cancer, and the HPV vaccine must be provided to undergraduate women, especially targeting those who are sexually inexperienced. In addition, educational programs must be developed to focus on the efficacy, safety, and benefits of the HPV vaccine.
In conclusion, despite the ability of the HPV vaccine to protect against cervical cancer, over 40% of undergraduate Taiwanese women have a low intention to obtain the HPV vaccine. Affordability of the HPV vaccine appears to be a barrier to vaccination. Free access to vaccination may improve the vaccination rate.
2. Jeng CJ, Ko ML, Ling QD, et al. Prevalence of cervical human papillomavirus in Taiwanese women. Clin Invest Med 2005; 28:261–266.
3. Brown DR, Shew ML, Qadadri B, et al. A longitudinal study of genital human papillomavirus infection in a cohort of closely followed adolescent women. J Infect Dis 2005; 191:182–192.
4. Munoz N, Bosch FX, de Sanjose S, et al. Epidemiologic classification of human papillomavirus types associated with cervical cancer. N Engl J Med 2003; 348:518–527.
5. Bosch FX, Lorincz A, Munoz N, et al. The causal relation between human papillomavirus and cervical cancer. J Clin Pathol 2002; 55:244–265.
7. The Future II Study Group. Prophylactic efficacy of a quadrivalent human papillomavirus (HPV) vaccine in women with virological evidence of HPV infection. J Infect Dis 2007; 196:1438–1446.
8. Harper DM, Franco EL, Wheeler CM, et al. Sustained efficacy up to 4.5 years of a bivalent L1 virus-like particle vaccine against human papillomavirus types 16 and 18: Follow-up from a randomized control trial. Lancet 2006; 367:1247–1255.
9. La Torre G, de Waure C, Chiaradia G, et al. HPV vaccine efficacy in preventing persistent cervical HPV infection: A systematic review and meta-analysis. Vaccine 2007; 25:8352–8358.
10. Rosenstock IM, Strecher VJ, Becker MH. Social learning theory and the health belief model. Health Educ Q 1988; 15:175–183.
11. Rosenstock IM, Strecher VJ, Becker MH. The health belief model and HIV risk behavior change. In: Diclemente RJ, Peterson JL, eds. Preventing AIDS: Theories and Methods of Behavioral interventions. New York, NY: Plenum Press, 1994:5–24.
12. Kahn JA, Rosenthal SL, Hamann T, et al. Attitudes about human papillomavirus vaccine in young women. Int J STD AIDS 2003; 14:300–306.
13. Slomovitz BM, Sun CC, Frumovitz M, et al. Are women ready for the HPV vaccine? Gynecol Oncol 2006; 103:151–154.
14. Boehner CW, Howe SR, Bernstein DI, et al. Viral sexually transmitted disease vaccine acceptability among college students. Sex Transm Dis 2003; 30:774–778.
15. Olshen E, Woods ER, Austin SB, et al. Parental acceptance of the human papillomavirus vaccine. J Adolesc Health 2005; 37:248–251.
16. Wang PD, Lin RS. Epidemiology of cervical cancer in Taiwan. Gynecol Oncol 1996; 62:344–352.
17. Gerend MA, Lee SC, Shepherd JE. Predictors of human papillomavirus vaccination acceptability among underserved women. Sex Transm Dis 2007; 34:468–471.
18. Kahn JA, Rosenthal SL, Jin Y, et al. Vaccine-type HPV infection and post-licensure attitudes about HPV vaccination in young women. J Adolesc Health 2008; 42:S28–S29.
19. Hoover DR, Carfioli B, Moench EA. Attitudes of adolescent/young adult women toward human papillomavirus vaccination and clinical trials. Health Care Women Int 2000; 21:375–391.
20. Holcomb B, Bailey JM, Crawford K, et al. Adults’ knowledge and behaviors related to human papillomavirus infection. J Am Board Fam Pract 2004; 17:26–31.
21. Yacobi E, Tennant C, Ferrante J, et al. University students’ knowledge and awareness of HPV. Prev Med 1999; 28:535–541.
22. Jain N, Euler GL, Shefer A, et al. Human papillomavirus (HPV) awareness and vaccination initiation among women in the United States, National Immunization Survey-Adult 2007. Prev Med 2009; 48:426–431.
23. Giles M, Garland S. A study of women’s knowledge regarding human papillomavirus infection, cervical cancer and human papillomavirus vaccines. Aust N Z J Obstet Gynaecol 2006; 46:311–315.
24. Fazekas KI, Brewer NT, Smith JS. HPV vaccine acceptability in a rural Southern area. J Womens Health 2008; 17: 539–548.
25. Zimet GD, Perkins SM, Sturm LA, et al. Predictors of STI vaccine acceptability among parents and their adolescent children. J Adolesc Health 2005; 37:179–186.
26. Marlow LA, Waller J, Evans RE, et al. Predictors of interest in HPV vaccination: A study of British adolescents. Vaccine 2009; 27:2483–2488.
27. Rosenthal SL, Lewis LM, Succop PA, et al. College students’ attitudes regarding vaccination to prevent genital herpes. Sex Transm Dis 1999; 26:438–443.