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What college women know, think, and do about human papillomavirus (HPV) and HPV vaccine
Vaccine 31 (2013) 1370–1376
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What college women know, think, and do about human papillomavirus (HPV) and HPV vaccine Nop T. Ratanasiripong a,∗ , An-Lin Cheng b , Maithe Enriquez c a b c
School of Nursing, California State University, Dominguez Hills, CA, USA School of Nursing, University of Missouri-Kansas City, MO, USA Sinclair School of Nursing, University of Missouri-Columbia, MO, USA
a r t i c l e
i n f o
Article history: Received 10 October 2012 Received in revised form 19 December 2012 Accepted 1 January 2013 Available online 10 January 2013 Keywords: HPV vaccine Knowledge Attitude Subjective norms Perceived behavioral control Intention Vaccine uptake
a b s t r a c t Objectives: This cross-sectional study, guided by Ajzen’s Theory of Planned Behavior, aimed to identify factors that influence the decision to obtain an HPV vaccine among college women and to examine the relationships among these factors. Methods: An electronic self-administered survey was utilized to collect data. An email invitation was sent to 3074 college women attending a large, public university in southern California, aged between 18 and 26 years. The email directed the recipient to click on a link to a web-based survey if she wanted to participate in the study. Results: Participants in this study were college women (n = 384; 175 HPV non-vaccinees and 209 HPV vaccinees). Women in this study knew that a Pap test is still needed after HPV vaccination and that the HPV vaccine does not protect against other Sexually Transmitted Infections. Both non-vaccinees and vaccinees had positive attitudes about mandating HPV vaccine. Knowledge and attitudes toward the vaccine were not directly linked to the outcome predictors – intention to obtain the vaccine and vaccine uptake. Attitude about receiving HPV vaccine, subjective norms (complying with the expectations of others), and perceived behavioral control were correlated with the outcome predictors. Subjective norms consistently predicted intention to obtain HPV vaccine and vaccine uptake. Conclusions: A proposal to mandate the HPV vaccine among young girls/women was acceptable to this population. Vaccination promotion strategies to increase the vaccine uptake rate among the catch-up group (aged 13–26) should include attention to college women’s subjective norms. Health care provider’s recommendation and encouragement from significant others (i.e., mother and peers) are critical in order for the college women to obtain the vaccine. © 2013 Elsevier Ltd. All rights reserved.
1. Introduction Cervical cancer is the second most common cancer among women worldwide and over 300,000 women die from this cancer each year [1]. In the United States (US), 12,000 women are diagnosed with cervical cancer and 4000 women die from it each year [2]. Healthy People 2020, the United States’ 10-year agenda for improving the nation’s health, called for an increase in cervical cancer screening rate and a reduction in the rates of invasive cervical cancer and human papillomavirus (HPV) infections among women in the U.S. [3].
∗ Corresponding author at: P.O. Box 21390, Long Beach, CA 90801, USA. Tel.: +1 562 481 2932. E-mail addresses: [email protected] (N.T. Ratanasiripong), [email protected] (A.-L. Cheng), [email protected] (M. Enriquez). 0264-410X/$ – see front matter © 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.vaccine.2013.01.001
The development of cervical cancer nearly always begins with HPV infection [1]. More than 100 different HPV types have been identified and approximately thirty types infect the genital tissues. High-risk, oncogenic HPV types (e.g., HPV 16 and HPV 18) are responsible for 99.7% of all cervical cancers while low-risk HPV types (e.g., HPV 6 and HPV 11) can result in mild cervical abnormalities, genital and respiratory tract warts [4,5]. Approximately 20 million Americans ages 15–49 are currently infected with HPV and another six million females and males become newly infected each year [1]. In the female population, the prevalence of genital HPV infection peaks among women aged 20–24 years (44.8%) and gradually declines among women aged 25–59 years (19.6–27.5%) [41,42]. About 10% of women who contract high risk HPV types develop persistent infections that can cause cervical cancer and negative health outcomes [4]. While there is no cure for HPV infection, the opportunity for prevention of HPV infection occurred in 2006 when the first HPV vaccine (Gardasil® ) was approved for routine vaccination for girls aged 11–12 and “catch-up” vaccination
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among girls/women aged 13–26. In 2009, another HPV vaccine (Cervarix® ) was licensed for use in females aged 10–25 [6]. Both vaccines have high efficacy against HPV 16 and 18 related cervical, vulvar, and vaginal cancers and pre-cancer lesions [6]. Recently, HPV4 was also approved for use in males aged 9–26 for prevention of anal intraepithelial neoplasia, anal cancer, and genital warts [7]. Researchers have documented an increased awareness of HPV and HPV vaccine among college-aged women since the first HPV vaccine was released [8–10]. Three studies conducted among college students reported that 78.5–94.0% of college women had heard about HPV through various sources, especially from television and radio [9,30,37]. A study conducted in 2009 among 739 college women also reported that over 97% of college women who have not received the vaccine were aware of HPV and most female students (84%) knew that genital HPV infection is linked to cervical cancer [28]. However, national data from 2009 shows low vaccine uptake. For adolescents aged 13–17, 44.3% have received at least 1 dose and 26.7% have received 3 doses of HPV vaccine [11]. For women aged 19–26, 17.1% have received at least 1 dose of an HPV vaccine [12]. A literature review reported that, depending on the setting, the HPV vaccine completion rate is between 4–47% among college-aged women [13]. From these low uptake results, arose the question “why have college women not obtained the HPV vaccine despite the fact that most of them are sexually active (70–77%)?” [14,38]. Proposals to make HPV vaccination routine and mandatory for girls in the United States have raised concerns. Some politicians, religious groups, and advocacy groups believe that mandating the HPV vaccine may send mixed messages between abstinence and premarital sex, and create confusion about the need for continued Pap testing [15,16]. Concerns have been voiced by these same groups about whether receipt of HPV vaccine might also encourage unsafe sexual practices due to a misunderstanding that HPV vaccine prevents all sexually transmitted infections (STIs) [15,16]. A review of the literature found some inconsistency among research findings regarding the factors that influence HPV vaccine uptake [17]. Moreover, no study was found that directly examined what college women think about getting vaccinated against HPV and whether the HPV vaccine controversies that exist are indeed related to a woman’s decision to obtain the HPV vaccine [17]. The aim of this cross-sectional study was to identify factors that influence the decision to obtain an HPV vaccine among college women and to examine the relationships among these factors. The theory of planned behavior (TPB) guided this study as it has been widely used to understand health-related behaviors in various populations, including the college-aged population [18]. The TPB provided a framework for understanding the antecedents to HPV vaccine uptake [18]. The theory purports that a person’s behavior is determined by his/her intention to perform the behavior and that this intention is, in turn, a function of attitude toward the
Individual factors & Experiences: -Demographic -HPV knowledge -Attitudes toward HPV vaccine - Sexual history
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behavior, subjective norms (complying with the expectations of others), and perceived behavioral control [18]. Variables of interest to this study were: knowledge, attitudes toward HPV vaccine, demographic characteristics, and past behavioral experiences that may influence HPV vaccine related behaviors, subjective norms, and perceptions of control [18]. The study related variables and their relationships are illustrated in Fig. 1. For this study, attitude toward getting vaccinated against HPV was defined as a woman’s belief about the consequences of performing the behavior. Subjective norms were defined as a woman’s beliefs about how her significant others view the behavior in question. Perceived behavioral control was defined as a woman’s perceptions of her ability to perform a given behavior. 2. Methods 2.1. Study sample Female, undergraduate college students aged 18–26 who were enrolled at a large public university in California participated in this study. This age range was chosen because it represents the traditional age range of college students. The maximum age range also aligns with the age limit (26 years old) to receive the HPV vaccine. The study was approved by the University’s Institutional Review Board. A random sampling list of the students’ email addresses was requested through the University’s Enrollment Services. Based on the University’s records, the email addresses were sorted by the student’s self-identified ethnicities (Caucasian, Asian, Hispanic and African–American). Within each ethnicity, a random sample of 800 emails per ethnic group was generated using SPSS. However, only 674 emails could be generated for the African–American group as that was the total number of eligible participants, resulting in a total sample of 3074. 2.2. Data collection An email invitation asking recipients to participate in the study was sent to 3074 women at the university in February 2012. In the email invitation, the recipient was directed to click on a link to a web-based survey if she chose to participate. The survey began with an informed consent page. If the woman did not agree to participate, the webpage would automatically close. If the woman agreed to participate, she was directed to another page to complete the study questionnaire. Two email reminders were sent 1 week and 2 weeks after the initial invitation was sent, unless an individual requested to be removed from the email list. The web-based survey was closed 4 weeks after the invitation was sent out. The web-based survey consisted of an “HPV and HPV vaccine related Knowledge, Attitudes, and Behaviors” questionnaire and demographic, sexual history, and vaccine uptake questions. The
Attitude toward getting vaccinated against HPV
Subjective norms to comply with expectations of others
Intention to obtain HPV vaccine
Perceived behavioral control to obtain HPV vaccine Fig. 1. Study theoretical framework.
HPV vaccine uptake
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questionnaire was specifically constructed for this study using the questionnaire construction guidelines created by Dr. Icek Ajzen, who developed the TPB [19]. There were 9 true/false items of HPV/HPV vaccine knowledge. A semantic differential-scale was used to measure attitudes toward HPV vaccine (9 items) and attitude toward getting vaccinated against HPV (6 items). A five-point Likert scale was used to measure subjective norms (5 items), perceived behavioral control (4 items), and intention to obtain the vaccine (4 items). Only non-vaccinees answered intention to obtain the vaccine items. Cronbach’s coefficient alpha of attitudes toward HPV vaccine, attitude toward getting vaccinated against HPV, subjective norms, perceived behavioral control, and intention to obtain HPV vaccine scales were 0.82, 0.87, 0.72, 0.70, and 0.96, respectively. 2.3. Statistical analysis Descriptive statistics were used to examine participant characteristics by vaccination status. In order to compare the participant characteristics between the non-vaccinee and vaccinee group, chi-square and Fisher’s exact tests (for categorical data) and the t-test (for continuous data) were used. Point-biserial correlation coefficients were used to determine the correlations between indirect predictors, direct predictors, and vaccine uptake. Then, significant indirect predictors (age, ethnicity, age of first sexual intercourse) were entered as covariates in the first block and the 3 direct predictors were entered in the second block of hierarchical logistic regression model to predict vaccine uptake. To examine intention to obtain the vaccine, Pearson’s correlation coefficients were used to determine the correlations between indirect predictors, direct predictors, and the vaccination intention. Then, significant indirect predictors (HPV/HPV vaccine knowledge and attitudes toward HPV vaccine) were entered as covariates in the first block and 3 direct predictors were entered in the second block of hierarchical multiple regression model to predict intention to obtain the vaccine.
Table 1 Demographic and sexual history of vaccinees and non-vaccinees* .
Age Ethnicity Caucasian Asian Latino Black Other Religion Christianity Other None Insurance status Yes No Class major Health-related Non health-related Relationship status Single Dating Married Ever having sex Yes No Partners Men Women Both Age of first sex STI diagnosis Yes No Pap test status Abnormal Normal
Non-vaccinees
Vaccinees
p-Value
M = 21.1 (n = 164) (n = 173,%) 31.2 17.9 20.8 20.8 9.2 (n = 170,%) 63.5 11.8 24.7 (n = 171,%) 73.1 26.9 (n = 172,%) 32.6 67.4 (n = 174,%) 50.0 47.1 2.9 (n = 170,%) 72.9 27.1 (n = 124,%) 94.4 3.2 2.4 M = 17.6(n = 122) (n = 120,%) 17.5 82.5 (n = 76,%) 10.5 89.5
M = 20.4 (n = 189) (n = 202,%) 28.2 26.2 24.3 10.4 10.9 (n = 203,%) 59.6 13.3 27.1 (n = 203,%) 76.8 23.2 (n = 202,%) 33.7 66.3 (n = 209,%) 43.5 53.6 2.9 (n = 199,%) 77.4 22.6 (n = 149,%) 91.3 5.4 3.3 M = 16.7(n = 148) (n = 139,%) 16.5 83.5 (n = 98,%) 15.3 84.7
<0.001a 0.03b
0.74b
0.40b
0.82b
0.44b
0.32b
0.72c
<0.001a 0.84b
0.36b
Note: M: mean. * A number of responses (n) differ because the participants chose not to answer or inadvertently skipped the questions. a By independent t-test. b By chi-square test. c By fisher’s exact test.
3. Results Of the 3074 students who were invited to participate in the study, 10 emails returned with delivery failure notification. There were 486 respondents to the invitation, 1 student declined to participate in the study and one student requested to be taken off the email reminder list – representing a response rate to the survey of 15.8%. Of the remaining 484 participants, 13 (2.6%) failed on attention-testing items (which identified if the subjects paid attention when answering the survey questions), 2 participants did not complete any items on the survey after they agreed to participate, and 27 participants had more than 20% of items missing: resulting in 442 participants that qualified for inclusion in the study. A total of 389 (94.9%) participants had heard about HPV and HPV vaccine and, of these, 209 had received at least 1 dose of an HPV vaccine. There were 175 who reported not having initiated an HPV vaccine, and 5 preferred not to indicate their vaccine status – leaving 384 participants for further data analysis. 3.1. Participant demographic and sexual history A comparison of demographic characteristics between nonvaccinees and vaccinees indicated that vaccine uptake was significantly associated with age and ethnicity (p = 0.03 and 0.00, respectively) (Table 1). The majority (97.1%) of all participants, nonvaccinees and vaccines, were single or dating and 75% reported being sexually active. Most had never been diagnosed with an STI or
abnormal Pap test. HPV vaccine uptake was significantly associated with age of first sexual intercourse (p < 0.001) (Table 1).
3.2. Descriptions of the variables The mean score on the HPV/HPV vaccine knowledge questionnaire among non-vaccinees was 6.62 and among vaccinees was 6.76 (out of 9). Most participants (over 90.0%) in both groups knew that they still needed a routine Pap test after vaccination and that HPV vaccine does not protect against all STIs. However, knowledge of HPV causing genital warts and risk for transmitting HPV was low in both groups (see Table 2). Both non-vaccinees and vaccinees had positive attitudes about mandating HPV vaccine (M = 14.04 and 16.35, on a possible range of 3–21) and negative attitudes about calling the HPV vaccine an anti-cancer vaccine (M = 11.66 and 11.67) or a STI vaccine (M = 11.85 and 10.79, on the same possible range). In addition, non-vaccinees and vaccinees had positive attitudes toward vaccination against HPV (M = 30.25 and 33.73, on a possible range of 6–42). Both groups also had positive subjective norms, with the vaccinee group having more positive subjective norms (M = 12.91 and 15.22, on a possible range of 4–20). Both groups had strong perceived behavioral control. However, non-vaccinees had stronger perceived behavioral control than vaccinees (M = 17.36 and 16.16, on a possible range of 4–20).
N.T. Ratanasiripong et al. / Vaccine 31 (2013) 1370–1376 Table 2 HPV/HPV vaccine knowledge: percentages of correct answers. Knowledge statements
Non-vaccinees (n = 175)
Vaccinees (n = 209)
1. HPV can cause genital warts 2. HPV can cause cervical cancer 3. Most people with genital HPV have no visible signs or symptoms 4. Using a condom can provide partial protection against HPV 5. I can transmit HPV to my partner(s) even if I have no HPV symptoms 6. One out of two women will be diagnosed with HPV once in their lifetime 7. Only sexually active women should receive the HPV vaccine 8. Women who receive HPV vaccine do not need to get routine Pap smear/test 9. HPV vaccine protects against all sexually transmitted infections
46.9% 86.3% 81.7%
43.5% 88.5% 77.5%
65.7%
71.8%
81.7%
77.5%
42.9%
45.5%
73.1%
85.6%
90.3%
93.3%
93.7%
92.8%
3.3. Predictors of HPV vaccine uptake
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Table 4 Hierarchical multiple regression analysis summary for attitude toward getting vaccinated against HPV, subjective norms, and perceived behavioral control, controlling for HPV knowledge and attitudes toward HPV vaccine, predicting intention to obtain HPV Vaccine (n = 164a ). Variables
B
SEB
ˇ
Step1 Knowledge Attitudes: vaccine
.31 .21
.17 .03
.12 .53**
3.35
1.45
−.01 .21 .26 .47 .16 −4.71
.12 .02 .31 .08 .09 1.83
Constant Step 2 Knowledge Attitudes: vaccine Attitude: getting vaccinated Subjective norms Perceived behavioral control Constant
R2
R2
.31
.31
.66
.35
−.00 .09 .51** .33** .08
a Mahalonobis test indicated 11 multivariate outliers. Thus, 164 non-vaccinees were used in the analysis. **p < 0.01.
reasons were received and these were categorized and are seen in Table 5.
Attitudes about receiving HPV vaccine, subjective norms, and perceived behavioral control were significantly correlated with vaccine uptake. The Omnibus Test of Model Coefficients indicated that, when all six variables (age, ethnicity, age of first sexual intercourse, attitude toward getting vaccinated against HPV, subjective norms, perceived behavioral control) were considered together, the ability of the model to predict vaccine uptake was significant (2 = 51.88, df = 6, n = 246, p < 0.01). Approximately 19.0–25.4% of the variance in the vaccine uptake was accounted for by these six variables. After controlling for the indirect predictors, subjective norms and perceived behavioral control remained significant in the multivariate model. Table 3 presents the odds ratios, suggesting that the odds of obtaining an HPV vaccine increases as subjective norms increase and perceived behavioral control decreases. 3.4. Predictors of intention to obtain HPV vaccine among non-vaccinees When only HPV knowledge and attitudes toward HPV vaccine were entered in the multiple regression model, attitudes toward HPV vaccine significantly predicted intention to obtain the HPV vaccine, F (2, 161) = 35.68, p = 0.00, adjusted R2 = 0.31. When the three direct predictor variables (attitude toward getting vaccinated against HPV, subjective norms, and perceived behavioral control) were added, they significantly improved the prediction (R2 change = 0.35). The entire group of variables significantly predicted intention to obtain HPV vaccine, F (5, 158) = 60.15, p = 0.00, adjusted R2 = 0.65. However, only attitude toward getting vaccinated against HPV and subjective norms significantly contributed to the model (Table 4). Most (93.7%) of the non-vaccinees provided various reasons for not obtaining an HPV vaccine in the free-text comment box. Some non-vaccinees provided more than one reason. A total of 180
Table 3 Logistic regression predicting HPV vaccine uptake (n = 384). Variables
B
SE
Odds ratio
p-Value
Age Ethnicity Age of first sexual intercourse Attitude: getting vaccinated Subjective norms Perceived behavioral control
−.10 .06 −.14 .01 .23 −.19
.08 .11 .08 .02 .06 .06
.90 1.05 .87 1.01 1.26 .83
.22 .62 .07 .57 .00 .00
4. Discussion This study found that age and ethnicity were significantly associated with vaccine uptake while religion, class major, and health insurance status were not. Several studies had previously reported ethnicity to have no impact on vaccine uptake [20–22]. However, one study conducted among college women, reported that race was significantly associated with HPV vaccine initiation, with African–Americans less likely to report obtaining the vaccine [23]. In addition, this study found that age of first sexual intercourse was associated with vaccine uptake while relationship status, sexual experience (i.e. ever having sex), partner genders, STI diagnosis history, and Pap test status were not. The study findings suggest that having sexual activity at an earlier age may raise a young woman’s awareness of the need for STI/HPV prevention. However, prior studies inconsistently showed that vaccine uptake was not associated with age of first sexual intercourse, relationship status, STI diagnosis history, and sexual experience [20,21,24]. Two Table 5 Reasons for not obtaining an HPV vaccine. Reasons
Frequency
%
Low risk perception (one partner, consistent condom use, “no need”) Not a priority (“never thought about it”, no motivation, laziness, distraction, too busy, “no specific reason”) Need of more vaccine information (on vaccine efficacy and safety) Cost and/or no insurance coverage Health care providers (having not suggested it, having not seen a doctor) General dislike toward shots (fear or dislike of shots, hospital) Never having had sexual intercourse Waiting to obtain the vaccine (already scheduled for vaccination) Mother/parents advised not to obtain the vaccine Scare of vaccine side effects (through news or friends) Having been already diagnosed with HPV Vaccine coverage (not preventing all HPV strains or all STIs) Misc. (not knowing where to get the vaccine, HPV infection is not serious, possible complications with other medical issues)
39
21.7
31
17.2
28
15.6
24 16
13.3 8.9
8
4.4
7 7
3.9 3.9
6 4
3.3 2.2
4 3
2.2 1.7
3
1.7
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studies conducted among women younger than 26 years old at a teen health center/health clinics, reported an association between the vaccine uptake and Pap test status [21,25]. Based on TPB, inconsistency of association findings between demographic, sexual history, and vaccine uptake might be because these variables did not directly influence the vaccine uptake [26]. 4.1. Indirect Predictors of HPV Vaccine Uptake This study found that both vaccinee and non-vaccinee groups had adequate HPV/HPV vaccine related knowledge. Consistent with previous studies that have been conducted with young women at various universities [27–30], over 90% of college women in both groups knew that routine Pap tests need to be continued after the vaccination. Women also knew that HPV vaccine does not protect against other STIs. These findings dispel the myths that college women might not seek routine Pap testing and might place themselves at higher risk for STIs because of misunderstandings about the need for Pap testing after the vaccination and that HPV vaccine covered all STIs. When the first HPV vaccine became available in 2006, it brought with it not only the first primary prevention method against cervical cancer, but also controversies over vaccine promotion and marketing strategies [16]. This study found that both non-vaccinees and vaccinees did not support the idea of calling HPV vaccine an anti-cancer or an STI vaccine. However, both groups, especially the vaccinee group favored a proposal to mandate the vaccine. Thus, mandating the vaccine through legislation would be acceptable to this population. A mandate, with an opt-out option, may be an appropriate strategy to increase the HPV vaccine uptake rate. Promoting the vaccine as an anti-cancer vaccine or an STI vaccine might be a disadvantage. Findings identified several important correlates of vaccine uptake and ruled out questionable correlates. HPV/HPV vaccine knowledge was not significantly correlated with HPV vaccine uptake. In accordance with the TPB, the findings confirmed that knowledge is not directly linked to a behavior – HPV/HPV vaccine knowledge alone is not sufficient to motivate vaccination. Thus, interventions to increase the vaccination uptake rate among college women should not focus on knowledge. 4.2. Direct predictors of HPV vaccine uptake The findings indicated that both vaccinees and non-vaccinees view getting vaccinated against HPV as desirable and beneficial. Both groups believed that significant others would want/wanted them to obtain the vaccine and that their health care providers would support them to do so. Furthermore, both groups also had strong perceived behavioral control: they believed that obtaining the vaccine was within their control. This study found that HPV vaccine uptake was significantly positively correlated with attitude toward getting vaccinated against HPV and subjective norms. However, the vaccine uptake was unexpectedly negatively correlated with perceived behavioral control: the vaccine uptake rate increased when the perceived behavioral control decreased. The findings also revealed that HPV vaccine uptake was predicted by subjective norms and perceived behavioral control. Currently, there is no available literature that has reported the specific examination of the association between vaccine uptake and attitude toward getting vaccinated against HPV. A few studies conducted among women aged 18–26, found that HPV vaccine uptake was positively related to some types of attitudes or beliefs (i.e., risk perceptions, HPV vaccine importance) [25,31,32]. Studies have also reported positive associations between vaccine uptake and subjective norms related-factors such as normative beliefs [21], approval from peers [24], approval from mother [32],
vaccine discussion with provider [23], and provider recommendation [33]. Findings consistently suggest that efforts to increase HPV vaccine uptake should be made through increasing positive attitudes toward getting vaccinated against HPV and subjective norms, especially subjective norms. Health care provider’s recommendation and encouragement from significant others (i.e., mother and peers) are also critical to the college woman’s decision to obtain an HPV vaccine. For the association between vaccine uptake and perceived behavioral control, the vaccinees tended to report significantly lower perceived behavioral control when compared to the non-vaccinees. This finding was consistent with the theory’s assumptions. However, this unexpected outcome might have occurred because perceived behavioral control was examined after vaccine administration. In other words, it appeared that the actual experience of getting vaccinated raised women’s perceptions of the difficulties or barriers involved, thereby lowering perceived behavioral control.
4.3. Predictors of intention to obtain HPV vaccine among non-vaccinees Intention to obtain HPV vaccine was positively significantly correlated with the indirect predictors (HPV/HPV vaccine knowledge and attitudes toward HPV vaccine) and direct predictors (attitude toward getting vaccinated against HPV, subjective norms, and perceived behavioral control). This finding is consistent with two prior studies which found that intention to obtain HPV vaccine was positively correlated with HPV knowledge, normative beliefs, and social norms, and inversely correlated with perceived barriers [9,34]. A study conducted among female college students between 2007 and 2009 also found that intention to obtain HPV vaccine was positively correlated with perceived parental approval, perceive risk, and perceived benefit from the vaccine [35]. However, for the current study, when indirect and direct variables were entered into the prediction model of intention to obtain HPV vaccine, only attitude toward getting vaccinated against HPV and subjective norms significantly contributed to the prediction model. This finding confirmed the TPB assumption that the influence of indirect variables is mediated by the direct predictors. Hence, to increase intention to obtain HPV vaccine among the catch-up group, efforts should be made to increase positive subjective norms and attitudes toward getting vaccinated against HPV. Vaccination promotion programs (e.g., flyers, TV advertisements, radio announcement, social network media) targeting health care providers, parents, and social norms may be beneficial. Furthermore, interventions that incorporate strategies to increase favorable attitudes toward getting vaccinated against HPV through changing some behavioral beliefs such as risk perception, may also be effective. Some non-vaccinees that participated in this study believed that they were not at risk/had low risk of acquiring HPV and some did not place vaccination as their priority. However, most participants (75%) were sexually active with an average number of four sexual partners in their lifetime. In addition, while most of non-vaccinees knew that HPV can cause cervical cancer and be asymptomatic, less than a half of them knew that HPV also causes genital warts and 50% of women will be diagnosed with HPV once in their lifetime [36]. A lack of knowledge could contribute to incorrect behavioral beliefs about perceived risk and perceived severity of HPV, which could impact one’s attitude about HPV vaccination. Hence, disseminating facts about the risks of HPV infection, as a part of HPV vaccination promotion programs, may also be beneficial. When women understand their risk and HPV severity, they may put vaccination at a higher priority.
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5. Conclusion This study’s findings must be interpreted within the context of the following limitations. This was a convenience sample of college women from one university; hence findings may not be generalizable. Self-reported data can be subjected to reporting and recall bias. Finally, a low response rate may be subjected to non-response bias. A bi-model response curve may have occurred due to a higher representation of the extremes [39,40]. Despite its limitations, this research provides new and important information that contribute to the understanding of HPV vaccine uptake rates. Findings from this study suggest that college women have positive attitudes toward getting vaccinated against HPV. While vaccine uptake and intention to obtain HPV vaccine are correlated with attitude toward getting vaccinated, subjective norms, and perceived behavioral control, subjective norms consistently predicts intention to obtain HPV vaccine and vaccine uptake. Health promotion programs to increase the vaccine uptake rate should certainly include attention to college women’s subjective norms. Attention to strengthen non-vaccinated college women’s behavioral beliefs, including correcting risk perception may also increase attitude toward getting vaccinated and, in turn, increase the vaccination uptake rate. The study also suggests that college women have positive attitude toward mandatory vaccination. Mandating vaccination, with an opt-out option may be appropriate to increase the vaccine uptake rate. Further research is needed to gain insight and strengthen the evidence and to further examine the relationship between vaccine uptake and attitude toward getting vaccinated against HPV. Potential research might include: (1) A qualitative study using a focus group method to seek deeper understanding about why college women do not perceive themselves at risk for HPV infection and why some women decide not to get vaccinated against HPV, (2) An experimental design study to examine the effectiveness of the HPV vaccine promotion program tailored to increase subjective norms. These study findings provide a research-based foundation for the development of clinical practice interventions to increase the number of young women who receive the HPV vaccine. Increasing HPV vaccine uptake will in turn reduce the rate of HPV infection, and decrease cervical cancer and negative HPV-related health outcomes.
Acknowledgements The American Nurses Foundation and the Pacific Coast College Health Association provided fuding for this study. The content of this paper is solely the responsibility of the authors and does not necessarily represent the official views of the funding agencies. The funders did not take part in the study design, data collection, analysis, interpretation, and report. This study was also supported by California State University– Long Beach, Student Services Division’ s administrators and staff in order to collect the data with the college women.
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[12] Center of Disease Control and Prevention. Statistics and surveillance: 2009 adult vaccination coverage, NHIS. 2011; http://www.cdc.gov/vaccines/ stats-surv/nhis/2009-nhis.htm [accessed 01.05.12]. [13] Sheinfeld Gorin SN, Glenn B, Perkins RB. The human papillomavirus (HPV) vaccine and cervical cancer: Uptake and next steps. Adv Ther 2011;28(8): 615–39. [14] The Kinsey Institute. Frequently asked sexuality questions to the Kinsey Institute. 2011; http://www.kinseyinstitute.org/resources/FAQ.html [accessed 01.05.11]. [15] Hager DW. Human papillomavirus infection and prevention in the adolescent population. J Pediatr Adolesc Gynecol 2009;22:197–204. [16] Vamos CA, McDermott RJ, Daley EM. The HPV vaccine: framing the arguments for and against mandatory vaccination of all middle school girls. J Sch Health 2008;78(6):302–9. [17] Ratanasiripong NT. Review of human papillomavirus (HPV) infection and HPV vaccine-related attitudes and sexual behaviors among college-aged women in the U.S. J Am Coll Health 2012;60(6):461–70. [18] Ajzen I. The theory of planned behavior. Organ Behav Hum Decis Process 1991;50(2):179–211. [19] Ajzen I. Constructing a theory of planned behavior questionnaire. 2010; http://people.umass.edu/aizen/pdf/tpb.measurement.pdf [accessed 01.05.11]. [20] Caskey R, Lindau ST, Alexander GC. Knowledge and early adoption of the HPV vaccine among girls and young women: results of a national survey. J Adolesc Health 2009;45(1):453–62. [21] Conroy K, Rosenthal SL, Zimet GD, et al. Human papillomavirus vaccine uptake, predictors of vaccination, and self-reported barriers to vaccination. J Womens Health 2009;18(10):1679–86. [22] Rosenthal SL, Weiss TW, Zimet GD, Ma L, Good MB, Vichnin MD. Predictors of HPV vaccine uptake among women aged 19–26: importance of a physician’s recommendation. Vaccine 2010;29(5):890–5. 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Vaccine journal homepage: www.elsevier.com/locate/vaccine
What college women know, think, and do about human papillomavirus (HPV) and HPV vaccine Nop T. Ratanasiripong a,∗ , An-Lin Cheng b , Maithe Enriquez c a b c
School of Nursing, California State University, Dominguez Hills, CA, USA School of Nursing, University of Missouri-Kansas City, MO, USA Sinclair School of Nursing, University of Missouri-Columbia, MO, USA
a r t i c l e
i n f o
Article history: Received 10 October 2012 Received in revised form 19 December 2012 Accepted 1 January 2013 Available online 10 January 2013 Keywords: HPV vaccine Knowledge Attitude Subjective norms Perceived behavioral control Intention Vaccine uptake
a b s t r a c t Objectives: This cross-sectional study, guided by Ajzen’s Theory of Planned Behavior, aimed to identify factors that influence the decision to obtain an HPV vaccine among college women and to examine the relationships among these factors. Methods: An electronic self-administered survey was utilized to collect data. An email invitation was sent to 3074 college women attending a large, public university in southern California, aged between 18 and 26 years. The email directed the recipient to click on a link to a web-based survey if she wanted to participate in the study. Results: Participants in this study were college women (n = 384; 175 HPV non-vaccinees and 209 HPV vaccinees). Women in this study knew that a Pap test is still needed after HPV vaccination and that the HPV vaccine does not protect against other Sexually Transmitted Infections. Both non-vaccinees and vaccinees had positive attitudes about mandating HPV vaccine. Knowledge and attitudes toward the vaccine were not directly linked to the outcome predictors – intention to obtain the vaccine and vaccine uptake. Attitude about receiving HPV vaccine, subjective norms (complying with the expectations of others), and perceived behavioral control were correlated with the outcome predictors. Subjective norms consistently predicted intention to obtain HPV vaccine and vaccine uptake. Conclusions: A proposal to mandate the HPV vaccine among young girls/women was acceptable to this population. Vaccination promotion strategies to increase the vaccine uptake rate among the catch-up group (aged 13–26) should include attention to college women’s subjective norms. Health care provider’s recommendation and encouragement from significant others (i.e., mother and peers) are critical in order for the college women to obtain the vaccine. © 2013 Elsevier Ltd. All rights reserved.
1. Introduction Cervical cancer is the second most common cancer among women worldwide and over 300,000 women die from this cancer each year [1]. In the United States (US), 12,000 women are diagnosed with cervical cancer and 4000 women die from it each year [2]. Healthy People 2020, the United States’ 10-year agenda for improving the nation’s health, called for an increase in cervical cancer screening rate and a reduction in the rates of invasive cervical cancer and human papillomavirus (HPV) infections among women in the U.S. [3].
∗ Corresponding author at: P.O. Box 21390, Long Beach, CA 90801, USA. Tel.: +1 562 481 2932. E-mail addresses: [email protected] (N.T. Ratanasiripong), [email protected] (A.-L. Cheng), [email protected] (M. Enriquez). 0264-410X/$ – see front matter © 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.vaccine.2013.01.001
The development of cervical cancer nearly always begins with HPV infection [1]. More than 100 different HPV types have been identified and approximately thirty types infect the genital tissues. High-risk, oncogenic HPV types (e.g., HPV 16 and HPV 18) are responsible for 99.7% of all cervical cancers while low-risk HPV types (e.g., HPV 6 and HPV 11) can result in mild cervical abnormalities, genital and respiratory tract warts [4,5]. Approximately 20 million Americans ages 15–49 are currently infected with HPV and another six million females and males become newly infected each year [1]. In the female population, the prevalence of genital HPV infection peaks among women aged 20–24 years (44.8%) and gradually declines among women aged 25–59 years (19.6–27.5%) [41,42]. About 10% of women who contract high risk HPV types develop persistent infections that can cause cervical cancer and negative health outcomes [4]. While there is no cure for HPV infection, the opportunity for prevention of HPV infection occurred in 2006 when the first HPV vaccine (Gardasil® ) was approved for routine vaccination for girls aged 11–12 and “catch-up” vaccination
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among girls/women aged 13–26. In 2009, another HPV vaccine (Cervarix® ) was licensed for use in females aged 10–25 [6]. Both vaccines have high efficacy against HPV 16 and 18 related cervical, vulvar, and vaginal cancers and pre-cancer lesions [6]. Recently, HPV4 was also approved for use in males aged 9–26 for prevention of anal intraepithelial neoplasia, anal cancer, and genital warts [7]. Researchers have documented an increased awareness of HPV and HPV vaccine among college-aged women since the first HPV vaccine was released [8–10]. Three studies conducted among college students reported that 78.5–94.0% of college women had heard about HPV through various sources, especially from television and radio [9,30,37]. A study conducted in 2009 among 739 college women also reported that over 97% of college women who have not received the vaccine were aware of HPV and most female students (84%) knew that genital HPV infection is linked to cervical cancer [28]. However, national data from 2009 shows low vaccine uptake. For adolescents aged 13–17, 44.3% have received at least 1 dose and 26.7% have received 3 doses of HPV vaccine [11]. For women aged 19–26, 17.1% have received at least 1 dose of an HPV vaccine [12]. A literature review reported that, depending on the setting, the HPV vaccine completion rate is between 4–47% among college-aged women [13]. From these low uptake results, arose the question “why have college women not obtained the HPV vaccine despite the fact that most of them are sexually active (70–77%)?” [14,38]. Proposals to make HPV vaccination routine and mandatory for girls in the United States have raised concerns. Some politicians, religious groups, and advocacy groups believe that mandating the HPV vaccine may send mixed messages between abstinence and premarital sex, and create confusion about the need for continued Pap testing [15,16]. Concerns have been voiced by these same groups about whether receipt of HPV vaccine might also encourage unsafe sexual practices due to a misunderstanding that HPV vaccine prevents all sexually transmitted infections (STIs) [15,16]. A review of the literature found some inconsistency among research findings regarding the factors that influence HPV vaccine uptake [17]. Moreover, no study was found that directly examined what college women think about getting vaccinated against HPV and whether the HPV vaccine controversies that exist are indeed related to a woman’s decision to obtain the HPV vaccine [17]. The aim of this cross-sectional study was to identify factors that influence the decision to obtain an HPV vaccine among college women and to examine the relationships among these factors. The theory of planned behavior (TPB) guided this study as it has been widely used to understand health-related behaviors in various populations, including the college-aged population [18]. The TPB provided a framework for understanding the antecedents to HPV vaccine uptake [18]. The theory purports that a person’s behavior is determined by his/her intention to perform the behavior and that this intention is, in turn, a function of attitude toward the
Individual factors & Experiences: -Demographic -HPV knowledge -Attitudes toward HPV vaccine - Sexual history
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behavior, subjective norms (complying with the expectations of others), and perceived behavioral control [18]. Variables of interest to this study were: knowledge, attitudes toward HPV vaccine, demographic characteristics, and past behavioral experiences that may influence HPV vaccine related behaviors, subjective norms, and perceptions of control [18]. The study related variables and their relationships are illustrated in Fig. 1. For this study, attitude toward getting vaccinated against HPV was defined as a woman’s belief about the consequences of performing the behavior. Subjective norms were defined as a woman’s beliefs about how her significant others view the behavior in question. Perceived behavioral control was defined as a woman’s perceptions of her ability to perform a given behavior. 2. Methods 2.1. Study sample Female, undergraduate college students aged 18–26 who were enrolled at a large public university in California participated in this study. This age range was chosen because it represents the traditional age range of college students. The maximum age range also aligns with the age limit (26 years old) to receive the HPV vaccine. The study was approved by the University’s Institutional Review Board. A random sampling list of the students’ email addresses was requested through the University’s Enrollment Services. Based on the University’s records, the email addresses were sorted by the student’s self-identified ethnicities (Caucasian, Asian, Hispanic and African–American). Within each ethnicity, a random sample of 800 emails per ethnic group was generated using SPSS. However, only 674 emails could be generated for the African–American group as that was the total number of eligible participants, resulting in a total sample of 3074. 2.2. Data collection An email invitation asking recipients to participate in the study was sent to 3074 women at the university in February 2012. In the email invitation, the recipient was directed to click on a link to a web-based survey if she chose to participate. The survey began with an informed consent page. If the woman did not agree to participate, the webpage would automatically close. If the woman agreed to participate, she was directed to another page to complete the study questionnaire. Two email reminders were sent 1 week and 2 weeks after the initial invitation was sent, unless an individual requested to be removed from the email list. The web-based survey was closed 4 weeks after the invitation was sent out. The web-based survey consisted of an “HPV and HPV vaccine related Knowledge, Attitudes, and Behaviors” questionnaire and demographic, sexual history, and vaccine uptake questions. The
Attitude toward getting vaccinated against HPV
Subjective norms to comply with expectations of others
Intention to obtain HPV vaccine
Perceived behavioral control to obtain HPV vaccine Fig. 1. Study theoretical framework.
HPV vaccine uptake
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questionnaire was specifically constructed for this study using the questionnaire construction guidelines created by Dr. Icek Ajzen, who developed the TPB [19]. There were 9 true/false items of HPV/HPV vaccine knowledge. A semantic differential-scale was used to measure attitudes toward HPV vaccine (9 items) and attitude toward getting vaccinated against HPV (6 items). A five-point Likert scale was used to measure subjective norms (5 items), perceived behavioral control (4 items), and intention to obtain the vaccine (4 items). Only non-vaccinees answered intention to obtain the vaccine items. Cronbach’s coefficient alpha of attitudes toward HPV vaccine, attitude toward getting vaccinated against HPV, subjective norms, perceived behavioral control, and intention to obtain HPV vaccine scales were 0.82, 0.87, 0.72, 0.70, and 0.96, respectively. 2.3. Statistical analysis Descriptive statistics were used to examine participant characteristics by vaccination status. In order to compare the participant characteristics between the non-vaccinee and vaccinee group, chi-square and Fisher’s exact tests (for categorical data) and the t-test (for continuous data) were used. Point-biserial correlation coefficients were used to determine the correlations between indirect predictors, direct predictors, and vaccine uptake. Then, significant indirect predictors (age, ethnicity, age of first sexual intercourse) were entered as covariates in the first block and the 3 direct predictors were entered in the second block of hierarchical logistic regression model to predict vaccine uptake. To examine intention to obtain the vaccine, Pearson’s correlation coefficients were used to determine the correlations between indirect predictors, direct predictors, and the vaccination intention. Then, significant indirect predictors (HPV/HPV vaccine knowledge and attitudes toward HPV vaccine) were entered as covariates in the first block and 3 direct predictors were entered in the second block of hierarchical multiple regression model to predict intention to obtain the vaccine.
Table 1 Demographic and sexual history of vaccinees and non-vaccinees* .
Age Ethnicity Caucasian Asian Latino Black Other Religion Christianity Other None Insurance status Yes No Class major Health-related Non health-related Relationship status Single Dating Married Ever having sex Yes No Partners Men Women Both Age of first sex STI diagnosis Yes No Pap test status Abnormal Normal
Non-vaccinees
Vaccinees
p-Value
M = 21.1 (n = 164) (n = 173,%) 31.2 17.9 20.8 20.8 9.2 (n = 170,%) 63.5 11.8 24.7 (n = 171,%) 73.1 26.9 (n = 172,%) 32.6 67.4 (n = 174,%) 50.0 47.1 2.9 (n = 170,%) 72.9 27.1 (n = 124,%) 94.4 3.2 2.4 M = 17.6(n = 122) (n = 120,%) 17.5 82.5 (n = 76,%) 10.5 89.5
M = 20.4 (n = 189) (n = 202,%) 28.2 26.2 24.3 10.4 10.9 (n = 203,%) 59.6 13.3 27.1 (n = 203,%) 76.8 23.2 (n = 202,%) 33.7 66.3 (n = 209,%) 43.5 53.6 2.9 (n = 199,%) 77.4 22.6 (n = 149,%) 91.3 5.4 3.3 M = 16.7(n = 148) (n = 139,%) 16.5 83.5 (n = 98,%) 15.3 84.7
<0.001a 0.03b
0.74b
0.40b
0.82b
0.44b
0.32b
0.72c
<0.001a 0.84b
0.36b
Note: M: mean. * A number of responses (n) differ because the participants chose not to answer or inadvertently skipped the questions. a By independent t-test. b By chi-square test. c By fisher’s exact test.
3. Results Of the 3074 students who were invited to participate in the study, 10 emails returned with delivery failure notification. There were 486 respondents to the invitation, 1 student declined to participate in the study and one student requested to be taken off the email reminder list – representing a response rate to the survey of 15.8%. Of the remaining 484 participants, 13 (2.6%) failed on attention-testing items (which identified if the subjects paid attention when answering the survey questions), 2 participants did not complete any items on the survey after they agreed to participate, and 27 participants had more than 20% of items missing: resulting in 442 participants that qualified for inclusion in the study. A total of 389 (94.9%) participants had heard about HPV and HPV vaccine and, of these, 209 had received at least 1 dose of an HPV vaccine. There were 175 who reported not having initiated an HPV vaccine, and 5 preferred not to indicate their vaccine status – leaving 384 participants for further data analysis. 3.1. Participant demographic and sexual history A comparison of demographic characteristics between nonvaccinees and vaccinees indicated that vaccine uptake was significantly associated with age and ethnicity (p = 0.03 and 0.00, respectively) (Table 1). The majority (97.1%) of all participants, nonvaccinees and vaccines, were single or dating and 75% reported being sexually active. Most had never been diagnosed with an STI or
abnormal Pap test. HPV vaccine uptake was significantly associated with age of first sexual intercourse (p < 0.001) (Table 1).
3.2. Descriptions of the variables The mean score on the HPV/HPV vaccine knowledge questionnaire among non-vaccinees was 6.62 and among vaccinees was 6.76 (out of 9). Most participants (over 90.0%) in both groups knew that they still needed a routine Pap test after vaccination and that HPV vaccine does not protect against all STIs. However, knowledge of HPV causing genital warts and risk for transmitting HPV was low in both groups (see Table 2). Both non-vaccinees and vaccinees had positive attitudes about mandating HPV vaccine (M = 14.04 and 16.35, on a possible range of 3–21) and negative attitudes about calling the HPV vaccine an anti-cancer vaccine (M = 11.66 and 11.67) or a STI vaccine (M = 11.85 and 10.79, on the same possible range). In addition, non-vaccinees and vaccinees had positive attitudes toward vaccination against HPV (M = 30.25 and 33.73, on a possible range of 6–42). Both groups also had positive subjective norms, with the vaccinee group having more positive subjective norms (M = 12.91 and 15.22, on a possible range of 4–20). Both groups had strong perceived behavioral control. However, non-vaccinees had stronger perceived behavioral control than vaccinees (M = 17.36 and 16.16, on a possible range of 4–20).
N.T. Ratanasiripong et al. / Vaccine 31 (2013) 1370–1376 Table 2 HPV/HPV vaccine knowledge: percentages of correct answers. Knowledge statements
Non-vaccinees (n = 175)
Vaccinees (n = 209)
1. HPV can cause genital warts 2. HPV can cause cervical cancer 3. Most people with genital HPV have no visible signs or symptoms 4. Using a condom can provide partial protection against HPV 5. I can transmit HPV to my partner(s) even if I have no HPV symptoms 6. One out of two women will be diagnosed with HPV once in their lifetime 7. Only sexually active women should receive the HPV vaccine 8. Women who receive HPV vaccine do not need to get routine Pap smear/test 9. HPV vaccine protects against all sexually transmitted infections
46.9% 86.3% 81.7%
43.5% 88.5% 77.5%
65.7%
71.8%
81.7%
77.5%
42.9%
45.5%
73.1%
85.6%
90.3%
93.3%
93.7%
92.8%
3.3. Predictors of HPV vaccine uptake
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Table 4 Hierarchical multiple regression analysis summary for attitude toward getting vaccinated against HPV, subjective norms, and perceived behavioral control, controlling for HPV knowledge and attitudes toward HPV vaccine, predicting intention to obtain HPV Vaccine (n = 164a ). Variables
B
SEB
ˇ
Step1 Knowledge Attitudes: vaccine
.31 .21
.17 .03
.12 .53**
3.35
1.45
−.01 .21 .26 .47 .16 −4.71
.12 .02 .31 .08 .09 1.83
Constant Step 2 Knowledge Attitudes: vaccine Attitude: getting vaccinated Subjective norms Perceived behavioral control Constant
R2
R2
.31
.31
.66
.35
−.00 .09 .51** .33** .08
a Mahalonobis test indicated 11 multivariate outliers. Thus, 164 non-vaccinees were used in the analysis. **p < 0.01.
reasons were received and these were categorized and are seen in Table 5.
Attitudes about receiving HPV vaccine, subjective norms, and perceived behavioral control were significantly correlated with vaccine uptake. The Omnibus Test of Model Coefficients indicated that, when all six variables (age, ethnicity, age of first sexual intercourse, attitude toward getting vaccinated against HPV, subjective norms, perceived behavioral control) were considered together, the ability of the model to predict vaccine uptake was significant (2 = 51.88, df = 6, n = 246, p < 0.01). Approximately 19.0–25.4% of the variance in the vaccine uptake was accounted for by these six variables. After controlling for the indirect predictors, subjective norms and perceived behavioral control remained significant in the multivariate model. Table 3 presents the odds ratios, suggesting that the odds of obtaining an HPV vaccine increases as subjective norms increase and perceived behavioral control decreases. 3.4. Predictors of intention to obtain HPV vaccine among non-vaccinees When only HPV knowledge and attitudes toward HPV vaccine were entered in the multiple regression model, attitudes toward HPV vaccine significantly predicted intention to obtain the HPV vaccine, F (2, 161) = 35.68, p = 0.00, adjusted R2 = 0.31. When the three direct predictor variables (attitude toward getting vaccinated against HPV, subjective norms, and perceived behavioral control) were added, they significantly improved the prediction (R2 change = 0.35). The entire group of variables significantly predicted intention to obtain HPV vaccine, F (5, 158) = 60.15, p = 0.00, adjusted R2 = 0.65. However, only attitude toward getting vaccinated against HPV and subjective norms significantly contributed to the model (Table 4). Most (93.7%) of the non-vaccinees provided various reasons for not obtaining an HPV vaccine in the free-text comment box. Some non-vaccinees provided more than one reason. A total of 180
Table 3 Logistic regression predicting HPV vaccine uptake (n = 384). Variables
B
SE
Odds ratio
p-Value
Age Ethnicity Age of first sexual intercourse Attitude: getting vaccinated Subjective norms Perceived behavioral control
−.10 .06 −.14 .01 .23 −.19
.08 .11 .08 .02 .06 .06
.90 1.05 .87 1.01 1.26 .83
.22 .62 .07 .57 .00 .00
4. Discussion This study found that age and ethnicity were significantly associated with vaccine uptake while religion, class major, and health insurance status were not. Several studies had previously reported ethnicity to have no impact on vaccine uptake [20–22]. However, one study conducted among college women, reported that race was significantly associated with HPV vaccine initiation, with African–Americans less likely to report obtaining the vaccine [23]. In addition, this study found that age of first sexual intercourse was associated with vaccine uptake while relationship status, sexual experience (i.e. ever having sex), partner genders, STI diagnosis history, and Pap test status were not. The study findings suggest that having sexual activity at an earlier age may raise a young woman’s awareness of the need for STI/HPV prevention. However, prior studies inconsistently showed that vaccine uptake was not associated with age of first sexual intercourse, relationship status, STI diagnosis history, and sexual experience [20,21,24]. Two Table 5 Reasons for not obtaining an HPV vaccine. Reasons
Frequency
%
Low risk perception (one partner, consistent condom use, “no need”) Not a priority (“never thought about it”, no motivation, laziness, distraction, too busy, “no specific reason”) Need of more vaccine information (on vaccine efficacy and safety) Cost and/or no insurance coverage Health care providers (having not suggested it, having not seen a doctor) General dislike toward shots (fear or dislike of shots, hospital) Never having had sexual intercourse Waiting to obtain the vaccine (already scheduled for vaccination) Mother/parents advised not to obtain the vaccine Scare of vaccine side effects (through news or friends) Having been already diagnosed with HPV Vaccine coverage (not preventing all HPV strains or all STIs) Misc. (not knowing where to get the vaccine, HPV infection is not serious, possible complications with other medical issues)
39
21.7
31
17.2
28
15.6
24 16
13.3 8.9
8
4.4
7 7
3.9 3.9
6 4
3.3 2.2
4 3
2.2 1.7
3
1.7
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studies conducted among women younger than 26 years old at a teen health center/health clinics, reported an association between the vaccine uptake and Pap test status [21,25]. Based on TPB, inconsistency of association findings between demographic, sexual history, and vaccine uptake might be because these variables did not directly influence the vaccine uptake [26]. 4.1. Indirect Predictors of HPV Vaccine Uptake This study found that both vaccinee and non-vaccinee groups had adequate HPV/HPV vaccine related knowledge. Consistent with previous studies that have been conducted with young women at various universities [27–30], over 90% of college women in both groups knew that routine Pap tests need to be continued after the vaccination. Women also knew that HPV vaccine does not protect against other STIs. These findings dispel the myths that college women might not seek routine Pap testing and might place themselves at higher risk for STIs because of misunderstandings about the need for Pap testing after the vaccination and that HPV vaccine covered all STIs. When the first HPV vaccine became available in 2006, it brought with it not only the first primary prevention method against cervical cancer, but also controversies over vaccine promotion and marketing strategies [16]. This study found that both non-vaccinees and vaccinees did not support the idea of calling HPV vaccine an anti-cancer or an STI vaccine. However, both groups, especially the vaccinee group favored a proposal to mandate the vaccine. Thus, mandating the vaccine through legislation would be acceptable to this population. A mandate, with an opt-out option, may be an appropriate strategy to increase the HPV vaccine uptake rate. Promoting the vaccine as an anti-cancer vaccine or an STI vaccine might be a disadvantage. Findings identified several important correlates of vaccine uptake and ruled out questionable correlates. HPV/HPV vaccine knowledge was not significantly correlated with HPV vaccine uptake. In accordance with the TPB, the findings confirmed that knowledge is not directly linked to a behavior – HPV/HPV vaccine knowledge alone is not sufficient to motivate vaccination. Thus, interventions to increase the vaccination uptake rate among college women should not focus on knowledge. 4.2. Direct predictors of HPV vaccine uptake The findings indicated that both vaccinees and non-vaccinees view getting vaccinated against HPV as desirable and beneficial. Both groups believed that significant others would want/wanted them to obtain the vaccine and that their health care providers would support them to do so. Furthermore, both groups also had strong perceived behavioral control: they believed that obtaining the vaccine was within their control. This study found that HPV vaccine uptake was significantly positively correlated with attitude toward getting vaccinated against HPV and subjective norms. However, the vaccine uptake was unexpectedly negatively correlated with perceived behavioral control: the vaccine uptake rate increased when the perceived behavioral control decreased. The findings also revealed that HPV vaccine uptake was predicted by subjective norms and perceived behavioral control. Currently, there is no available literature that has reported the specific examination of the association between vaccine uptake and attitude toward getting vaccinated against HPV. A few studies conducted among women aged 18–26, found that HPV vaccine uptake was positively related to some types of attitudes or beliefs (i.e., risk perceptions, HPV vaccine importance) [25,31,32]. Studies have also reported positive associations between vaccine uptake and subjective norms related-factors such as normative beliefs [21], approval from peers [24], approval from mother [32],
vaccine discussion with provider [23], and provider recommendation [33]. Findings consistently suggest that efforts to increase HPV vaccine uptake should be made through increasing positive attitudes toward getting vaccinated against HPV and subjective norms, especially subjective norms. Health care provider’s recommendation and encouragement from significant others (i.e., mother and peers) are also critical to the college woman’s decision to obtain an HPV vaccine. For the association between vaccine uptake and perceived behavioral control, the vaccinees tended to report significantly lower perceived behavioral control when compared to the non-vaccinees. This finding was consistent with the theory’s assumptions. However, this unexpected outcome might have occurred because perceived behavioral control was examined after vaccine administration. In other words, it appeared that the actual experience of getting vaccinated raised women’s perceptions of the difficulties or barriers involved, thereby lowering perceived behavioral control.
4.3. Predictors of intention to obtain HPV vaccine among non-vaccinees Intention to obtain HPV vaccine was positively significantly correlated with the indirect predictors (HPV/HPV vaccine knowledge and attitudes toward HPV vaccine) and direct predictors (attitude toward getting vaccinated against HPV, subjective norms, and perceived behavioral control). This finding is consistent with two prior studies which found that intention to obtain HPV vaccine was positively correlated with HPV knowledge, normative beliefs, and social norms, and inversely correlated with perceived barriers [9,34]. A study conducted among female college students between 2007 and 2009 also found that intention to obtain HPV vaccine was positively correlated with perceived parental approval, perceive risk, and perceived benefit from the vaccine [35]. However, for the current study, when indirect and direct variables were entered into the prediction model of intention to obtain HPV vaccine, only attitude toward getting vaccinated against HPV and subjective norms significantly contributed to the prediction model. This finding confirmed the TPB assumption that the influence of indirect variables is mediated by the direct predictors. Hence, to increase intention to obtain HPV vaccine among the catch-up group, efforts should be made to increase positive subjective norms and attitudes toward getting vaccinated against HPV. Vaccination promotion programs (e.g., flyers, TV advertisements, radio announcement, social network media) targeting health care providers, parents, and social norms may be beneficial. Furthermore, interventions that incorporate strategies to increase favorable attitudes toward getting vaccinated against HPV through changing some behavioral beliefs such as risk perception, may also be effective. Some non-vaccinees that participated in this study believed that they were not at risk/had low risk of acquiring HPV and some did not place vaccination as their priority. However, most participants (75%) were sexually active with an average number of four sexual partners in their lifetime. In addition, while most of non-vaccinees knew that HPV can cause cervical cancer and be asymptomatic, less than a half of them knew that HPV also causes genital warts and 50% of women will be diagnosed with HPV once in their lifetime [36]. A lack of knowledge could contribute to incorrect behavioral beliefs about perceived risk and perceived severity of HPV, which could impact one’s attitude about HPV vaccination. Hence, disseminating facts about the risks of HPV infection, as a part of HPV vaccination promotion programs, may also be beneficial. When women understand their risk and HPV severity, they may put vaccination at a higher priority.
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5. Conclusion This study’s findings must be interpreted within the context of the following limitations. This was a convenience sample of college women from one university; hence findings may not be generalizable. Self-reported data can be subjected to reporting and recall bias. Finally, a low response rate may be subjected to non-response bias. A bi-model response curve may have occurred due to a higher representation of the extremes [39,40]. Despite its limitations, this research provides new and important information that contribute to the understanding of HPV vaccine uptake rates. Findings from this study suggest that college women have positive attitudes toward getting vaccinated against HPV. While vaccine uptake and intention to obtain HPV vaccine are correlated with attitude toward getting vaccinated, subjective norms, and perceived behavioral control, subjective norms consistently predicts intention to obtain HPV vaccine and vaccine uptake. Health promotion programs to increase the vaccine uptake rate should certainly include attention to college women’s subjective norms. Attention to strengthen non-vaccinated college women’s behavioral beliefs, including correcting risk perception may also increase attitude toward getting vaccinated and, in turn, increase the vaccination uptake rate. The study also suggests that college women have positive attitude toward mandatory vaccination. Mandating vaccination, with an opt-out option may be appropriate to increase the vaccine uptake rate. Further research is needed to gain insight and strengthen the evidence and to further examine the relationship between vaccine uptake and attitude toward getting vaccinated against HPV. Potential research might include: (1) A qualitative study using a focus group method to seek deeper understanding about why college women do not perceive themselves at risk for HPV infection and why some women decide not to get vaccinated against HPV, (2) An experimental design study to examine the effectiveness of the HPV vaccine promotion program tailored to increase subjective norms. These study findings provide a research-based foundation for the development of clinical practice interventions to increase the number of young women who receive the HPV vaccine. Increasing HPV vaccine uptake will in turn reduce the rate of HPV infection, and decrease cervical cancer and negative HPV-related health outcomes.
Acknowledgements The American Nurses Foundation and the Pacific Coast College Health Association provided fuding for this study. The content of this paper is solely the responsibility of the authors and does not necessarily represent the official views of the funding agencies. The funders did not take part in the study design, data collection, analysis, interpretation, and report. This study was also supported by California State University– Long Beach, Student Services Division’ s administrators and staff in order to collect the data with the college women.
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