JOURNAL OF WOMENS HEALTH Volume 19, Number 7, 2010 Mary Ann Liebert, Inc. DOI: 10.1089/jwh.2009.

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Adult Womens Attitudes Toward the HPV Vaccine

1,2 1,2 Mary B. Short, Ph.D., Susan L. Rosenthal, Ph.D.,3 Lynne Sturm, Ph.D.,4 Lora Black, M.A., 1 5 4 Melissa Loza, B.A., Daniel Breitkopf, M.D., and Gregory D. Zimet, Ph.D.

Abstract

Aims: Two human papillomavirus (HPV) vaccines have demonstrated efcacy in preventing HPV infection and are currently being administered to adolescent girls in several countries. Although the most efcient HPV prevention strategy is immunizing adolescents before there is any risk of exposure, adult women also may benet from vaccination. This study aimed to explore the attitudes of women aged 2755 years toward the HPV vaccine. Methods: Thirty-eight women were recruited from a university-based gynecological practice, completed a demographic questionnaire, and then were interviewed. Results: Most participants had heard about the vaccine and were positive about the HPV vaccine for adult women. Women advocated universal access to this vaccine, indicating that all women should have the option. They assessed their risk level in several ways, including level of monogamy, relationship status, previous sexual risk behaviors, history of an abnormal Pap smear, and family history. All but 2 woman described barriers to vaccination, including cost, side effects, and hassle factors. Most women did not believe the vaccine would change risk behaviors. Conclusions: The women from this convenience sample knew the HPV vaccine existed and in general found it acceptable. If an HPV vaccine becomes available to adult women, healthcare professionals will be faced with the challenge of providing accurate information, being sensitive and willing to help each individual woman make a decision, and being creative when developing new ways to eliminate barriers to getting the vaccine.

Introduction

he prevalence of high-risk human papillomavirus (HPV) types is as much as 13% in women over 30.1 Women and their infants can have serious consequences as a result of HPV infection. High-risk HPV types are associated with cervical cancer, which is the second most common cancer in women worldwide; specically, types 16 and 18 are responsible for approximately 70% of cervical cancers. The incidence of oropharyngeal and tonsillar cancers is estimated to be 0.321.5 males/0.02.8 females per 100 person-years,2 and HPV 16 is believed to cause about one third of those cancers.3 Another consequence of HPV infection is genital warts, most commonly caused by HPV 6 and HPV 11. For women, the prevalence of genital warts peaks between ages 20 and 24 years but remains a problem for older women, with new cases being identied in women >50 years.4 In addition, vertical

transmission of HPV can lead to recurrent respiratory papillomatosis (RRP), causing obstruction of the airway, stridor, progressive hoarseness, and respiratory distress.5 There are two HPV vaccines that have demonstrated efcacy in preventing HPV infection and are currently licensed and recommended to be administered to adolescent girls in several countries.69 In some countries, such as Australia, the quadrivalent vaccine has been licensed for administration to boys. Both HPV vaccines target the two most common types of HPV associated with cervical cancer (16 and 18), and one of the HPV vaccines also prevents the two types of HPV associated with the majority of genital wart infections (6 and 11).8 The HPV vaccines are not therapeutic vaccines; therefore, they need to be given before exposure in order to confer benet. The quadrivalent HPV vaccine protects against both low (6 and 11) and high (16 and 18) types of HPV, and both HPV vaccines may provide cross-protection to other high-risk

1 2

Department Department 3 Department 4 Department 5 Department

of of of of of

Pediatrics, University of Texas Medical Branch, Galveston, Texas. Psychology, University of Houston at Clear Lake, Houston, Texas. Pediatrics, Columbia University School of Medicine, New York, New York. Pediatrics, Indiana University School of Medicine, Indianapolis, Indiana. Obstetrics and Gynecology, University of Texas Medical Branch, Galveston, Texas.

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1306 types. Thus, only if a woman has been infected with all types covered by the HPV vaccine will she not obtain some benet from vaccination. Even though both HPV vaccines are not licensed to be administered to those >26 years of age, both HPV vaccine manufacturers will seek licensure for women >26 years of age,9 and there is some off-label use of the quadrivalent vaccine for older women. These women could still benet from either vaccine as long as they have remained uninfected with one or more vaccine-related HPV types. HPV vaccines could be an effective strategy to prevent infectious diseases, and previous research has demonstrated that the HPV vaccine is likely to be acceptable to adult women. Women who believe they are vulnerable to HPV or cervical cancer,1012 who have many partners,13 and who are younger are more likely to nd the HPV vaccine acceptable.14,15 Even if women nd the HPV vaccine acceptable, there will be barriers (both traditional and potentially novel) to immunizing adult women. Further, there has been concern that the HPV vaccine may have unintended negative consequences such as less frequent Papanicolaou (Pap) smear screening or increased risky sexual behavior, even though there is no evidence to support this concern. The current study extends the ndings from previous studies by using in-depth interviews with women who are 2755 years of age about how women dene the need for the HPV vaccine, determine risk for themselves or others, perceive barriers, and assess the postvaccine behavior. Materials and Methods Women (n 38) who were patients in a university-based gynecological practice were recruited from November 2007 through May 2008. Recruitment was accomplished in two ways. First, iers were placed throughout the clinic, and women were asked to call the research ofce number if they were interested in participating. Once they called the research ofce, an appointment was scheduled for an interview. Even though all patients could potentially see the iers, only employees were responding to iers; therefore, a second recruitment method was implemented. The second recruitment method included having a research coordinator approach women waiting for appointments. Because other demands on the time of the research staff, a researcher was available to approach women in the waiting room only 5 days during the months of April and May. Once a woman agreed to participate, the interview was conducted; when it was completed, another woman was recruited. Overall, 2 to 5 women were recruited and interviewed each day. Any English-speaking woman between the ages of 27 and 55 who received health care from the clinic was eligible to participate. Women who worked in the clinic were allowed to participate as long as they also obtained care from the clinic. Of the 21 women approached in the waiting room of the clinic who were eligible to participate, 6 declined. Three of the patients reported not having time, and 3 did not give a reason. The participants completed a demographics questionnaire that assessed such information as age, educational level, and sexual and medical history and then were interviewed using a semistructured interview. During the interview, before answering any HPV-specic questions, the women received information about the HPV vaccine, its targeted strains, and

SHORT ET AL. the possibility of licensure for women >26 years. These interviews were taped and transcribed, and the transcriptions were checked for accuracy. Women were asked if they had heard of the HPV vaccine, who they thought should be immunized, what barriers might prevent women from getting the vaccine, and how they believed women would make a decision to be immunized. All recruitment and study procedures were approved by the Institutional Review Board at the University of Texas Medical Branch in Galveston. Consent was obtained from all participants before lling out the demographics questionnaire and participating in the interview. Framework analysis16 was used as the structure for analyzing the data. The transcribed tapes were reviewed to develop and organize themes for coding. The interviews then were coded using these themes, and the coding was reviewed for accuracy by at least two researchers. Discrepancies between the coders were discussed and resolved by consensus. New themes and coding were developed as the data were mapped to existing literature. Results Sample Overall, 38 women agreed to participate, and of these 38 participants, 15 were recruited through the clinic waiting room and 23 were recruited through iers posted in the gynecological clinic. Fifteen of the women had some employment association with the clinic: nurses/nursing assistants/ medical assistants (n 9), women who scheduled appointments (n 3), a research assistant (n 1), a patient caretaker (n 1), and a business ofce employee (n 1). Participants had a mean age of 40 years (range 2753 years) and a mean number of lifetime partners of 5 (range 150). The demographics of the women are presented in Table 1. HPV vaccine awareness The participants in the study were asked if they had heard of the HPV vaccine and, if so, the source of the information. Thirty-four of the 38 participants reported having heard of the vaccine; all 3 women with less than a high school education had not heard of the vaccine. Of the 30 participants who identied a source of information, 15 reported having heard of the vaccine through commercials, 4 from the news media about Texas Governor Perrys proposed HPV vaccination mandate, 7 through their work in a gynecological setting, and 4 from a variety of personal sources. The women were then given information about the HPV vaccines. The participants factual knowledge about HPV and the HPV vaccine was not systematically assessed; however, many of them spontaneously shared their understanding of the HPV vaccine. Those who had heard of the vaccine did not necessarily accurately describe transmission of HPV or HPVrelated diseases. For example, 1 participant, who said she had heard of the vaccine from the media, stated, This I dont think you can pass on to somebody else. You cant give this to somebody. You cant give cervical cancer to another person, as far as I know, you cant. Another participant who reported having heard of the vaccine said, That, just like any other vaccine, like the rubella or whatever, it helps, you know, to prevent. Not to prevent STD, but help to ght

WOMENS PERCEPTIONS OF HPV VACCINE Table 1. Demographics of Participants (n 38) Frequency Age, years 2535 3645 4655 Race African American Non-Hispanic white Hispanic Education High school or less Some college or more Relationship status Engaged/married/living together Single, sexually experienced Single, virgin Lifetime partners 0 13 46 79 >10 History of abnormal Pap smear History of genital warts History of cervical dysplasia 13 (34%) 14 (37%) 11(29%) 15 (40%) 14 (37%) 9 (23%) 14 (37%) 24 (63%) 22 (58%) 15 (39%) 1 (3%) 1 13 12 7 5 19 4 7 (3%) (34%) (32%) (18%) (13%) (50%) (11%) (18%)

1307 woman said, The ones who were at higher risk. The ones who really needed it per se. They had to be compromised, they had to be the elderly, they could be pregnant, you know in those categories. Another woman commented on the health status of women older than 55 by saying, They would because at that age youre really worried about everything. I know my sister is about that age, and she just wants to prevent anything she can prevent, before it starts going down hill. In contrast to these opinions, another woman stated, I would recommend it for all healthy women, women with healthy immune systems. Risk determination There were several factors that women considered in assessing the need to get vaccinated, including nonmonogamy, relationship status, previous sexual risk behaviors or abnormal Pap smear, and family history of cancer. As noted, participants sometimes thought that if a woman was concerned that her relationship was not monogamous, she should get vaccinated. Some participants believed that women know whether or not their relationship is monogamous, but others did not agree, illustrated by the woman who said, Because I dont think anybody believes their partner cheats on them until it happens. For the most part, women talked about their husbands or boyfriends having other partners, rather than women having additional partners. However, one acknowledged both possibilities as she said, I guess, if your husbands going to stray, or if you stray, or you know, whoever strays. Another situation for which women advocated vaccination involved being newly single as the result of divorce or death. Women believed vaccination was particularly applicable for women between 45 and 55 years of age and were less certain about it for women >55 years. One woman said that women >45 years would denitely want to get the vaccine, but then added about women over 55 years, I dont know cause, when youre 55, I feel like maybe they are just a little more settled in their life. Some women were more focused on womens previous sexual behaviors than current behaviors. One woman said, Im in a monogamous relationship, but I question some of the exposure that we might have from before. For 2 women this was based on the concept that the virus could be dormant. Another past risk that was of concern to women was a history of abnormal Pap smears. One woman said that she would get the vaccine because I had the abnormal Pap smear. Id like to take something that can possibly prevent me from getting anything else farther down the road. Another possible risk factor that women considered was family history. Several participants mentioned that women who had a family member with a history of female cancers should get vaccinated, but some broadened this to any type of cancer or noncancer illnesses, such as the woman who said, Maybe if cancer runs in their family. They got heredity or whatever. Or you know, their general risk for the usual stuff, I mean, as far as the people have high blood pressure, stroke. Barriers to vaccination All but 2 of the women described one or more potential barriers to getting a desired vaccine. The most common

infection from the women from the STD passing on to cervical cancer. Whom to vaccinate In general, women advocated universal access to this vaccine, often answering that all women should get it. However, despite believing that all women should get it, some women answered in a manner consistent with an optimistic bias, that is, the tendency to view others as at greater risk than themselves. These women, who stated that they would not get it themselves, typically relied on faith in the monogamy of their relationships to provide protection. In contrast, others said that even though they did not meet risk-based criteria for getting the vaccine, they would still get it. For example, one woman said:
I think it just depends on how sexually active that theyve been in the past. If theyve had a history of abnormal Pap in their past. But, Id get it and Im going to be in that age group, I would get it. But, Ive not been that very sexually [active] in my life. I got married to my husband who was my rst partner, and I was 17 years old, been married 25 years, so I havent had a history of having multiple partners in my life.

The rationale for believing in vaccinating all women included women not knowing what their risks might be, or a generally positive view of prevention, such as the woman who said, I mean, what if you were at the [shopping mall] and got raped in the parking garage or whatever. You know thats another thought. Im all for protection. Another woman described women who would get vaccinated as those women who may be more vigilant about their health. Women had contrasting views about the role of general health in the decision to get the vaccine. Some women thought that women with poorer health status should get it. As one

1308 barrier mentioned was nancial cost. Lack of insurance coverage for the vaccine, cost of transportation to the clinic, and general inability to pay out-of-pocket costs, such as copays, were described by nearly half the sample. The next most frequently cited barriers were concerns about potential shortterm and long-term side effects that might be associated with the vaccine and fear of needles. Fears of side effects ranged from concern about ill effects that might appear years after the vaccination (If somethings going to come back and bite them in the butt 10 years later) to fears about bodily disgurement and negative emotional reactions: If it made her sick. It if . . . left some kind of horrible scar . . . just if it affected her state of health at that moment. You know, if it made her crazy or something. Another woman wondered about potential long-term efcacy: Just cause shes scared, like me . . . are there going to be side effects, whats the long-term, how long is it going to last . . . for sure. Are you going to have to go back down the line, get a booster shot? With regard to fear of needles, some women said that although this was a barrier, women would still get the vaccine, but 1 woman suggested, I think the shot itself, mostly because theyre afraid of needles. . . . So, I think if they made it like in pill form instead of vaccine, something you could just take. Hassle factors, such as the competing demands from family, especially the needs of children, and daily responsibilities (i.e., work), were noted by some women. Another barrier mentioned by 6 women was negative opinions of others or lack of endorsement from physicians. Another woman believed that cultural mores and their partners fears that vaccination could lead women to be unfaithful might potentially play a role in some families. Changes in behaviors Women were told by the interviewer that some people were concerned that women would reduce their participation in Pap smear screening and increase sexual risk behaviors (i.e., sexual disinhibition or risk compensation) after vaccination. Most participants, however, viewed Pap smear screening behaviors as unlikely to be affected by vaccination. These women sometimes acknowledged that not all women were consistent in getting their Pap smears regularly, often linking this to poor education. Some women thought there was a possibility that womens Pap smear screening rates might decrease, but only a few linked it to a sense of decreased vulnerability. One woman said, They just probably dont care, they gure they got the vaccine and they are good to go. Another said, I think theyd be more condent that they wouldnt be getting cervical cancer so they let it go more times. Other women noted that women may forget or experience a general sense of lack of vulnerability because of family history or negative Pap smears in the past. Three women thought that women would increase their Pap smear behavior, but none of them provided a rationale for that belief,. The women who did not think women would change their behaviors often discussed the role of education, and 1 said she would not change her behavior, Just to validateits working! I dont have, I dont have this, because, you know, I got the shot. Similarly, most of the participants did not think that women would change their sexual behavior after vaccination, with some even reporting that the question did not

SHORT ET AL. make any sense. Some women thought that it was possible that there might be an increase in risky sexual behavior or a perception of an increase, but many of these women thought that the increase would be limited to select groups of individuals, such as younger or uneducated people or those from lower socioeconomic backgrounds. Some women thought that women might increase preventive sexual behaviors after vaccination. For example, 1 woman said, Because that vaccine is already like letting you know its a caution out there. So I would use a condom just in case, and another thought that women would have fewer partners, because the men dont tell you everything. But, a man probably dont know that they have it. One woman suggested that a side effect of the vaccine might be that vaccinated women would lose the feeling of wanting to have sex. It was not clear whether she believed this to be a biological or psychological side effect. Discussion Although vaccines have been the most effective strategy to prevent infectious diseases, their impact can be limited by poor uptake or changes in behavior after vaccination that lead to a different risk prole. Challenges to the implementation of HPV vaccination for adult women include poor knowledge, lack of acceptability among those at risk, barriers to receiving the vaccine, and concerns about postvaccine behavior. Similar to other studies, most women in this study had heard of the HPV vaccine, but some had mixed levels of knowledge and understanding.1719 Most of the participants source of information about HPV and the HPV vaccine was commercials or news report.20,21 Because information presented by media sources varies widely in its accuracy and detail,17,22 people may be misinformed or have difculty understanding the information provided. Thus, it is important that health professionals provide accurate and complete information and work with the media to insure that information provided is accurate, complete, and easy to understand. Critical information to communicate includes the preventive vs. therapeutic nature of the vaccine and that the vaccine could have value for women who have had HPV infection, as they are unlikely to have had all vaccine types. Further, given the common misperceptions that these women held about HPV and the HPV vaccine, educational efforts need to address these misperceptions (such as that cervical cancer is hereditary, that high-risk populations for the HPV vaccine may be different from the high-risk populations for other vaccines, such as u). Other studies have demonstrated that women want more information about this vaccine,20 and the need for more information has been cited as a reason for not choosing to have oneself or ones children vaccinated.23,24 Once information is provided, healthcare providers will need to help women determine their own risk. Although the women in this study advocated for universal availability, there was a variety of ways they would decide on a specic womans risk level and need for vaccination, including current relationship status, past risk behaviors and HPV status, and family history of cancer. It is interesting that many of the women thought that those with historical risk factors for infection should be vaccinated, but these are the women who stand to benet least from the vaccine, as they are most likely

WOMENS PERCEPTIONS OF HPV VACCINE to have already been exposed to one or more HPV types. Some participants thought women would base their decision on a general sense that any form of prevention is positive. Given the variety of decision-making processes identied, healthcare providers will need to help a given woman to consider her situation in light of the available evidence base about risk factors for infection and cervical cancer, as well as the degree of value the woman places on health protection in general. This approach may help a woman to evaluate her personal risk prole, the health protection benet she may, therefore, achieve with vaccination, and the indirect benet of reduction in health-related anxiety she might derive from choosing to be vaccinated. Once a woman decides to get vaccinated, she may still encounter barriers to accomplishing this goal. Similar to ndings of other studies on HPV vaccines and other vaccines, affordability was deemed to be an important factor in acceptability of the HPV vaccine.18,20,2527 For this vaccine to be covered by insurance, it is likely that a universal recommendation by the Advisory Committee on Immunization Practices (ACIP) would be necessary. It may be difcult to obtain universal recommendation given that current data suggest universal implementation for this age group may be not costeffective.28 As is the case with most vaccines, concerns about potential side effects were a commonly cited barrier.25,27,29 The clinical trial results of both the HPV vaccines suggest that the side effects are minimal, yet the HPV vaccine, similar to other vaccines, continues to receive negative coverage from the press. A related barrier reported was a fear of needles, which has also been described as a barrier for other vaccines.26,27,30 Given that the HPV vaccine requires a series of three shots, future availability of a needleless vaccine may be helpful in increasing womens comfort. One issue raised by the women in this study was the competing demands on their nances and time because of being a mother or taking care of others. Perhaps women could be vaccinated at work settings or in the pediatricians ofce when they take a child in for care. Adolescents from this same healthcare setting had completion rates of <60% for the threedose series,31 suggesting that it may be necessary to nd ways to enhance adherence to the three doses. This may be particularly helpful for women obtaining the vaccine in gynecology clinics, which may not have vaccine reminder systems set up. Perhaps, as healthcare providers schedule patients for the second and third doses, they should routinely problem solve with women about how to manage self-identied practical barriers to follow-through. The sexual transmissibility of HPV was not spontaneously mentioned as a barrier to acceptance by many women in this study. We did not explore the possibility that this was related to poor understanding of the sexual transmission of HPV. This nding is consistent with previous research examining parents attitudes toward vaccines for sexually transmitted infections (STI), which showed that parents were much more concerned about the efcacy and safety of the vaccine and not very focused on mode of transmission (sexual vs. nonsexual).32 However, decision making for ones child may differ from decision making for oneself. If vaccinated women either increased their exposure to HPV infection through riskier sexual behaviors or reduced the frequency of Pap smear screening, the impact of the vaccine

1309 might be substantially less than desired. For the most part, however, the women in this study did not indicate that either of these would be a common response, and some women appeared to think that the education associated with the vaccine would lead to adoption of less risky behaviors. Certainly, some adolescent medicine specialists have argued for the use of vaccines to enhance the delivery of preventive healthcare for adolescents.33 Perhaps HPV vaccinations could be used in a similar manner for adult women. In addition, either with or without HPV vaccination, some women will engage in risky sexual behavior or fail to get regular preventive gynecological examinations. Thus, the availability of the vaccine should not reduce our efforts to promote healthy behaviors among those women. It should be noted that this was a convenience sample of women, and several of them had some medical training or familiarity with gynecology. Therefore, the ndings from this study may not generalize to other groups of women. However, qualitative studies are used for gathering in-depth (often exploratory) data to guide further research and are not meant to be decisional or generalizable by nature. In addition, a high proportion of the sample had a history of a past abnormal Pap smear or cervical dysplasia. Thus, the women in this study may have been more knowledgeable than other women and more willing to receive the vaccine or think women should receive the vaccine. Women with the most limited HPV awareness/knowledge were those with lower levels of education. Nonetheless, misunderstandings about both HPV and HPV vaccine were quite common, although knowledge was not systematically assessed in this study. It is difcult, therefore, to determine if responses were actually based on a true understanding or misunderstanding of these issues. The women in this study were already connected to a gynecological healthcare setting and had overcome barriers to accessing reproductive healthcare; thus, the sample may represent a resourceful group of women who are able to negotiate the healthcare system and be proactive about their own healthcare. They may be biased to have positive health beliefs, including favorable attitudes toward the HPV vaccine. Follow-up quantitative surveys could assess the importance of anticipated barriers to vaccine access among adult women and determine if type of barrier is associated with demographic characteristics of respondents. If the HPV vaccines are licensed and made available to adult women, studies can test the disinhibition hypothesis, which proposes that some women may engage in more sexually risky behavior after vaccination.34 When reviewing the data from other health behaviors, however, the ACIP anticipates that disinhibition will be unlikely to result from the HPV vaccination.35 A recent study found that very few mothers and adolescents thought that getting the HPV vaccination would cause an increase in risky behavior.36 Despite the aforementioned limitations, our ndings suggest that adult women who have a source of gynecological care may be interested in HPV vaccination. If and when HPV vaccines are licensed for women aged >27, healthcare professionals will be faced with the challenge of providing accurate information to women with a variety of sexual histories and current and anticipated relationship situations. Additional research to develop interventions to decrease barriers associated with vaccination should include taking

1310 advantage of opportunities to vaccinate women at convenient times and locations. Acknowledgments We thank Heather Meza for her help in data collection and management. This study was funded by a grant from Merck Vaccine Division awarded to S.L.R. and D.Z. Disclosure Statement S.L.R. and G.D.Z. serve as research consultant/collaborators on a Merck-sponsored research project, and S.L.R. served on a Merck advisory board. The other authors have no conicts of interest to report. References
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Address correspondence to: Susan L. Rosenthal, Ph.D. Morgan Stanley Childrens Hospital Columbia University Medical Center 3959 Broadway 11th Floor, Room 1124 South New York, NY 10032 E-mail: slr2154@columbia.edu

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