HPV-Related Risk Perceptions and HPV Vaccine Uptake Among a Sample of Young Rural Women

Abstract

Appalachia Kentucky is recognized for increased cervical cancer incidence, morbidity and mortality and lower rates of Pap testing. Understanding the predictors of Human Papillomavirus (HPV) vaccine uptake is warranted among this population. The purpose of this exploratory research is to determine associations between HPV-related risk perceptions and uptake of free Gardasil offered to rural Appalachian women ages 18–26 attending regional health clinics. Young women (N = 247) were recruited from health clinics in Southeastern, Kentucky from March 2008 through September 2009. After completing a brief interview assessing seven HPV-related risk perceptions, women received a HPV vaccine voucher which provided the entire three-dose vaccine series free of charge. Whether women redeemed the voucher for dose one of Gardasil served as the study outcome variable. Hierarchical logistic regression was used to estimate the independent effects of each predictor variable on vaccine uptake. Less than 50% redeemed the voucher to receive dose one of the HPV vaccine. Five of the seven variables significantly predicted uptake. In a controlled analysis, only two predictors remained significant: “in general, vaccines are a good thing” (P = .02) and “I believe that getting the vaccine will be painful” (P = .03). The remaining three predictor variables (worry about having HPV [P = .07], HPV is serious enough for vaccination [P = .43], and not sure vaccine is safe [P = .22]) were not significant in the model. Health promotion programs designed for this population may enhance HPV vaccine uptake by creating more realistic perceptions about the inherent value of vaccines and by improving perceptions relative to injection pain.

Introduction

In the cancer domain much of the seminal research related to risk perception is focused on cancer screening and genetic testing [1–3]. However, with the introduction of the Human Papillomavirus (HPV) vaccine to protect against cervical cancer [4], cancer-related risk perception research can now be extended to include vaccination-based risk perception which has been previously focused on influenza, pneumonia, Hepatitis B, and Lyme Disease vaccines [5, 6]. This is an important line of research considering genital HPV has been identified as the most commonly sexually transmitted infection (STI) in the United States and HPV types 16 and 18 are responsible for over 70% of cervical cancers [4]. Dunne and colleagues estimate the prevalence of HPV infection among US females to be over 25% (approximately 25 million women), with women ages 20–24 experiencing the highest prevalence at 45% [7]. With the historical advent of the novel HPV vaccine––which demonstrates close to 100% efficacy in preventing precancerous cervical cell changes [4]––it is imperative to understand the predictors of uptake of this public health achievement, including HPV-related risk perceptions.

In assessing HPV-related risk perceptions and their impact on vaccination behavior, key constructs utilized in multiple health behavior theories can be readily applied including perceived worry about the infection, perceived threat (combination of perceived susceptibility and severity), perceived barriers and benefits, and associated risks of vaccination. However, much of the HPV-related risk perception research to date has focused primarily on vaccine acceptability, intentions to get the vaccine, and/or barriers to vaccination from the perspective of parents, young adolescents, the general public, and/or healthcare providers [8–17]. The most notable study conducted by Brewer and Fazekas utilized the health belief model as a guiding framework for a systematic review of HPV-related beliefs and vaccine acceptability and found vaccination acceptability to be higher among those who perceived the vaccine effective, believed a healthcare provider would recommend the vaccine, and considered HPV infection likely [8]. Less common in the literature are studies focused on risk-related predictors of HPV vaccine uptake (i.e., initiation of the three-dose regimen). Studies published to date have focused primarily on sociodemographic and clinical variables identified through medical records [18–20]. Furthermore, less attention has been given to the “catch up” pool of women ages 13–26 [4, 21, 22]. Many women over the age of 18 are no longer eligible for childhood vaccine programs, are often uninsured, and have not been the primary focus of HPV-related pharmaceutical marketing campaigns [23].

One population of women of particular interest are young adult females who live in rural, Appalachia Kentucky, a region recognized for higher rates of cervical cancer incidence and mortality, lower rates of Pap testing, and limited HPV awareness [9, 24–32]. Moreover, the region is also noted for a physical and socio-cultural environment (e.g., geographic isolation, lower socioeconomic status) which may preclude positive health outcomes [33–35]. Accordingly, the purpose of this exploratory study was to determine associations between HPV-related risk perceptions and uptake of dose one of Gardasil offered for free to rural Appalachian women 18–26 years of age attending local health clinics.

Methods

Study Sample

The geographic region chosen for this study is one of the few remaining areas in Appalachia containing a high concentration of “distressed counties” (42 out of 54 Kentucky Appalachian-designated counties) as classified by the Appalachian Regional Commission [36]. The area has some of the poorest counties in the nation [37].

From March 2008 through September 2009, a research assistant recruited female patients in any of five local health clinics located in five rural counties of Southeastern Kentucky. Women were eligible if they were not pregnant, 18–26 years old, and had not been vaccinated with Gardasil (the only HPV vaccine approved for use at the time). Of 249 eligible women, 247 (99%) agreed to participate in the study and provided written informed consent. The Institutional Review Board at the University of Kentucky approved the study protocol.

Procedures

Because Gardasil was not universally covered by insurance plans, it was determined that the study design would have to remove the barrier of cost to effectively determine associations between risk perceptions and Gardasil uptake. The fact that the entire three-dose regimen would be provided at no cost was not advertised or disclosed until after the questionnaire was completed. To avoid self-selection bias, the project was called the Women’s Health Study. Volunteers were told that, “the purpose of this survey is to learn more about why women would or would not accept the HPV vaccine if it was made available to them.” After providing consent, women completed a questionnaire via structured interview. Women were compensated with a $25 gift card for their time. The research assistant then provided women with a voucher to receive free Gardasil which could be redeemed at the clinic recruitment site. It should be noted that the voucher provided all three doses of the HPV vaccine at no cost to the women. These coupons were coded with an ID number that matched the ID number recorded on the women’s questionnaires. Redeemed coupons were used to track and document Gardasil uptake. The number of women redeeming the voucher for the initial dose of vaccine served as the study outcome variable.

Measures

The questionnaire was refined based on experiences in a previous study [38]. The questionnaire began with a brief paragraph that explained HPV and its role in cervical cancer. This paragraph included two sentences that let women know about the newly approved HPV vaccine. Seven questionnaire items specifically assessed women’s HPV-related risk perceptions. The first asked women, “How often do you worry that you might have HPV?” and response options were provided on a 4-point scale ranging from 1 “never” to 4 “frequently.” Women were then presented with six questions that used a 5-point response scale ranging from 1 “strongly agree” to 5 “strongly disagree.” These questions were: (1) “I consider HPV to be serious enough to justify getting the vaccine;” (2) “In the next year or two I am very likely to become infected by HPV;” (3) “I think the vaccine may cause minor side effects such as fatigue or fever;” (4) “I am not sure the HPV vaccine is safe;” (5) “In general vaccines are a good thing;” and (6) “I believe that getting the vaccine will be painful.” To ease data interpretation, items above marked #1 and #5 were reverse coded thereby meaning that higher scores on any of the seven items represented perceptions that were logically more favorable toward HPV vaccine uptake.

Statistical Analysis

Bivariate associations between the predictor variables and the outcome measure were assessed by independent samples t tests. Predictors achieving bivariate significance were entered into a two block hierarchical logistic regression model, using direct entry in the first block and forward Wald entry in the second block. To control for confounding, the first block contained only likely covariates: (1) penile-vaginal sex in the past 12 months, (2) having sex with two or more partners in the past 12 months, and (3) ever having an abnormal result on a Pap test. The second block contained the HPV-related risk perceptions achieving bivariate significance.

Results

Descriptive Findings

A total of 247 women were enrolled in the study. Of these 44.9% (n = 111) redeemed the coupon to receive dose one of Gardasil. Average age was 21.7 years (SD = 2.5). Table 1 displays descriptive characteristics of the sample. The majority were Caucasian (98.4%). Eighty-three percent of the women reported having penile-vaginal sex in the past 12 months. Gardasil uptake was not associated with this measure (P = .11). About one of every six women (16.2%) reported having penile-vaginal sex with two or more partners in the past 12 months. Gardasil uptake was not associated with this measure (P = .30). Over a quarter of women (27.1%) reported ever having an abnormal result on a Pap test. Gardasil uptake was significantly associated with this measure (P = .047), with 55.2% uptake among those ever having an abnormal Pap compared to 41.1% among remaining women. Uptake did not vary as a function of women’s age (P = .96). Thus, only the measure of ever having an abnormal Pap test result was used as an analytic covariate.

Table 1.

Descriptive characteristics of the study sample (N = 247)

Variable	n	%
Race
Caucasian/White	243	98.4
Asian	1	.4
Native American	1	.4
Other	2	.8
Hispanic Ethnicity	1	.4
Had penile-vaginal sex (past 12 months)	203	82.8
Had 2 or more penile-vaginal sex partners (past 12 months.)	40	16.2
Ever had an abnormal result on a Pap test	67	27.1

March 2008 through September 2009, Southeastern, Kentucky

Bivariate Associations

Table 2 displays the bivariate findings pertaining to the assessed HPV-related risk perceptions. As shown, all except two of the seven predictors achieved bivariate significance. The two groups of women (vaccine/no vaccine) did not differ with respect to perceived likelihood of being infected by HPV in the next 2 years. Also, the perception that the vaccine would cause minor side effects did not predict subsequent uptake of Gardasil.

Table 2.

Bivariate associations between HPV-related risk perceptions and HPV vaccine uptake (dose 1) (N = 247)

Predictor	Mean (vaccine)a	Mean (no vaccine)b	t c	P value
Worry about having HPVd	1.83	1.53	2.52	.013
Likely to be infected by HPVe	3.74	3.86	2.88	.38
HPV serious enough for vaccinef	4.36	4.17	2.01	.046
Vaccine may cause side effectsg	2.81	2.77	.39	.69
Not sure vaccine is safeh	3.39	3.14	2.22	.027
Vaccines are a good thingi	4.30	4.06	2.57	.01
The vaccine will be painfulj	3.52	3.20	2.73	.007

March 2008 through September 2009, Southeastern, Kentucky

^aAmong 111 young women receiving dose 1 of Gardasil

^bAmong 136 young women not receiving dose 1 of Gardasil

^cAll t values have 245 degrees of freedom

^dAssessed on a 4-point scale with “4” representing the most worry

^eAssessed on a 5-point scale with “5” representing greatest perceived likelihood

^fAssessed on a 5-point scale with “5” representing greatest agreement

^gAssessed on a 5-point scale with “5” representing least agreement

^hAssessed on a 5-point scale with “5” representing least agreement

ⁱAssessed on a 5-point scale with “5” representing greatest agreement

^jAssessed on a 5-point scale with “5” representing least agreement

Multivariate Associations

The model was significant (χ² with 3df = 14.96, P < .002) thus indicating the value of the entered variables. After controlling for ever having an abnormal Pap test, only two of the HPV-related risk perceptions remained significant in the multivariate model. For each unit (on a 5-point scale) of greater agreement that “in general, vaccines are a good thing” women were about 35% less likely to decline the free Gardasil (AOR = .65; 95% CI = .45–.95; P = .02). In other words, a young woman who indicated strong agreement (5) would be, for example, 70% less likely to decline than a woman who indicated uncertainty (3). Similarly, for each unit of greater agreement that “I believe that getting the vaccine will be painful”, women were about 27% less likely to decline the free Gardasil (AOR = .73; 95% CI = .55–.97; P = .03). In essence, women who thought the vaccine would be painful were reticent to actually get the vaccine. The remaining three predictor variables (worry about having HPV [P = .07], HPV is serious enough for vaccination [P = .43], and not sure vaccine is safe [P = .22]) were not significant in the model.

Discussion

Despite being offered dose one of the Gardasil vaccine for free in a healthcare setting, barely half of this rural, younger sample of women accepted the vaccine. These findings are counterintuitive to Hopenhayn’s findings that 92% of women, age 18–29, residing in two Appalachian Kentucky counties would accept the HPV vaccine for themselves [39] as well as Fazekas’ findings that 66% of women in rural North Carolina were more likely to get the vaccine if it was free [11].

Almost all of the women in the study indicated they had been sexually active in the past 12 months, with over 15% having sexual intercourse with two or more partners, putting themselves at risk for HPV infection. Notably, over 25% of the women reported an abnormal Pap test which was significantly associated with vaccine uptake corresponding to Crosby et al.’s research with college-aged women at two Kentucky universities [38]. In the bivariate analysis, worry about having HPV, perceived HPV severity, perceived vaccine safety, perceived value of the vaccine, and perceived pain were all significant predictors of Gardasil uptake. It was surprising to find perceived likelihood of HPV infection was not a significant predictor of vaccine uptake which differs from the results of Brewer and colleagues’ meta-analysis of the relationship between risk perception and vaccination behavior [5] and systematic review of vaccine acceptability [8]. Similarly, concern over vaccine side effects did not significantly impact uptake of dose one among this population.

Of five predictor variables achieving bivariate significance, only two remained significant in the multivariate model. A general belief that vaccines are “a good thing” and less concern about the pain from the injection each independently predicted Gardasil uptake in this population of young rural women. On the contrary, worry about having HPV, perceptions about severity of HPV justifying vaccination, and concerns about vaccine safety were not significant predictors of uptake.

May argues the preventive value of vaccines as well as their benefit to the larger population has been poorly communicated to the general public [40]. Public health communication campaigns fail to articulate the social and economic impact of diseases, including vaccines’ potential to dramatically reduce disease incidence and mortality, improve quality of life, and reduce related healthcare costs [41–43]. Additionally, more recent anti-vaccination movements related to the potential link between childhood vaccines and autism may influence the public’s negative or uncertain perceptions of vaccine safety [44]. Slonim and colleagues demonstrated adolescents and young adults in particular have very little general knowledge about vaccines [45]. Related specifically to Gardasil, misperceptions of the vaccine’s preventive value may stem from its novelty, connection to a STI, primary recommendation for young girls, higher costs, and uncertain impact on other HPV-related malignancies such as oropharyngeal and anogenital cancers [10, 12, 46]. Furthermore, sensationalized media reports related to the side effects of the HPV vaccine may impact women’s perception of the vaccine and future acceptance of it [47–49].

All of the above circumstances may be magnified in a rural, medically underserved region such as Appalachia where preventive care is often undervalued and underutilized [46, 50, 51]; health mis-information is often perpetuated through informal friend and family networks [52–54]; women’s health issues, Pap testing, and STIs are often considered too embarrassing to discuss [46, 54, 55]; religiosity and conservatism are prevalent [46, 54, 56]; and residents may experience lower socioeconomic status and lower rates of health literacy [34, 57, 58]. Unfortunately, many rural women may fail to comprehend the physical, mental, and economic consequences of developing genital warts and/or cervical cancer which could be prevented from receiving the three sequential doses of the HPV vaccine.

The most common vaccine side effect associated with Gardasil is pain at the injection site, followed by injection site swelling and erythema [59–61]. Pain has been associated with vaccine acceptability in previous HPV-vaccine related studies [16, 62]. However, Reiter and colleagues established that the pain associated with the HPV vaccine is equal to or less painful than other routine adolescent shots, specifically the meningococcal vaccine and the tetanus booster, according to parents’ recollections of their daughters’ vaccine experiences [63]. Appalachian women’s overall lack of knowledge of regarding cervical cancer, HPV, and the vaccine may contribute to the concern of pain from the injection [46, 54, 64].

Limitations and Study Strengths

Findings are limited by the use of a convenience sample, the cross-sectional nature of the interview, and the validity of the self-reported data. Notably our study population was recruited through local health clinics indicating they have access to healthcare; however, even within a healthcare setting only 45% of the women received dose one of Gardasil. The strengths of our research include a focus on the “catch up” pool of women, ages 18–26, rarely targeted by HPV vaccination campaigns as well as a medically underserved region of the United States, where the population has been termed, a “special population” and a “neglected minority” [34, 65, 66].

Conclusions

Keeping in mind these limitations and study strengths, the findings suggest that among rural women, 18–26 years of age, two modifiable factors may increase Gardasil uptake. Health promotion programs designed for this population may enhance HPV vaccine uptake by creating more realistic perceptions about the inherent value of vaccines to personal and public health. There is an obvious role for healthcare providers in educating and raising general vaccination awareness among their young adult, rural female patient population as well as provision of factual and logistical information related to the HPV vaccine [43, 46]. Programs should also attempt to instill improved perceptions relative to pain of injections. Young women may falsely believe that extreme pain will be experienced and they may too quickly dismiss the long-term benefits of vaccination in favor of avoiding only a moment of minor pain. In an age group where incidence of HPV is high and HPV vaccination rates are low (10%) [23], and in a rural population which experiences higher rates of cervical cancer and lower rates of screening, identification and intervention on risk-related perceptions may help to increase uptake of this important public health achievement to decrease cervical cancer incidence, mortality, and morbidity.