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Overcoming barriers to HPV vaccine acceptance.

The advent of preventive human papillomavirus (HPV) vaccines has created new opportunities for improved health care for women, which will require both patients and physicians to develop new paradigms and strategies to deal with HPV-related diseases. New thinking is needed to take advantage of our ability to prevent these diseases, instead of just treating the sequelae of HPV infections. Education and flank discussion of HPV-related diseases can set the foundation for understanding the role and potential benefits of HPV vaccines.

The first step toward helping our patients accept a new vaccine is to identify what people need to know about HPV, the diseases it causes, and the benefits of being vaccinated vs the risks associated with not being vaccinated. Educational efforts will also need to be directed toward the concerns of the parents of adolescents who could be the major beneficiaries of an HPV vaccination program. Finally, the psychosocial issues of symptomatic HPV infection and of potential target populations receiving the vaccine need to be discussed. Clearly, vaccination has been a successful prevention strategy for many diseases and has made the incidence of viral infections such as polio and smallpox a thing of the past.

What do women want to know about HPV?

Studies show that few individuals have a clear understanding of HPV and the consequences of infection. (1) Literature analyzing the concerns of women and their desire for information regarding HPV is limited. In a recent study, Anhang et al attempted to identify the most relevant educational information desired by women about HPV and HPV testing. (2) Forty-eight participants were included in this study; subjects were low-income, ethnically diverse women stratified by age (18-29, 30-54, and [greater than or equal to] 55 years). Study participants were asked to respond to a series of questions and paragraphs regarding many aspects of HPV infection. Incredibly, only 27% of the participants were familiar with HPV before the start of the focus group, even though 85% had received a Papanicolaou (Pap) test in the 2 years prior to the study. The principal information about HPV that women desired was related to transmission, prevention, treatment, and the degree of cervical cancer risk. Although information regarding these core areas was desired by women, regardless of age or ethnicity, women of different age-groups expressed some distinct interests. Typically, younger women focused on the symptoms associated with low-risk HPV infection, particularly the types that cause genital warts. Conversely, older women expressed concern about high-risk HPV infection, notably since high-risk HPV types are associated with cervical cancer. Across all age-groups, women were specifically interested in determining their personal HPV infection status and gaining a better understanding of risk factors (eg, age, sexual behaviors, sexual behaviors of previous sexual partners, and immunologic status) that contribute to susceptibility.

One of the findings of the study is that some women's fears centered on the lack of infallible techniques for the prevention of HPV transmission. This may be important in educating women about HPV vaccines since they could prevent the majority of the serious sequelae of HPV infections by the serotypes present in the vaccine. Although HPV vaccines are not infallible because they don't cover all HPV types, they may give women some comfort and a sense of control over the disease. Women also expressed confusion regarding HPV biology. Many women in the study had difficulty understanding the difference between low-risk and high-risk HPV types. Their confusion translated into uncertainty regarding the level of anxiety they may have if diagnosed with HPV. Some women were unclear about how HPV could be asymptomatic and how it could cause cervical cancer. However, most women felt the need to determine their HPV status, if possible.

Many women were confused by the significance of DNA screening for HPV compared with Pap test results. As a result, messages designed to educate women on HPV infection should describe not only HPV susceptibility according to both age and risk profiles but also what the results of molecular and cytologic tests mean. Messages should also clearly state the differences among HPV types (the association of HPV 16 and 18 with cervical cancer, and HPV 6 and 11 with anogenital warts) and their consequences, provide an accurate assessment of cancer risk, and emphasize the notion that proper screening practices can reduce this associated risk.

Attitudes of adolescent and young adult women toward HPV vaccination

The success of an HPV vaccination program ultimately depends on whether target vaccination groups are willing to be vaccinated. Adolescents, their parents (or guardian medical decision makers), and young adults will be involved in deciding whether or not to pursue vaccination. To successfully implement this disease prevention program, an accurate understanding of the attitudes, intentions, and level of understanding of HPV in these populations is needed. Unfortunately, knowledge about HPV among adolescents and young adults is also limited. In one study, only 8.3% of 15- to 17-year-old adolescents and 34.5% of 18- to 28-year-old women had heard of HPV. (3) In spite of this, the majority of women showed a positive attitude and distinct beliefs regarding the outcomes of HPV vaccination. In a study conducted by Zimet et al, in which the investigators analyzed attitudes toward 9 distinct and hypothetical HPV vaccines among 40 adult and adolescent women, vaccine efficacy, endorsement by physicians, and the cost of the vaccine were the major factors that determined the acceptability of an HPV vaccine. Additionally, mothers who indicated they would receive an HPV vaccine also wanted their teenage daughters to receive the vaccine. (4) Another study showed that women who indicated they would accept an HPV vaccine would also get it for their hypothetical 12-year-old daughter. (3)

Young adult women are very concerned about genital warts. In a study of 15- to 28-year-old women, concern about cervical cancer was high. Moreover, half of the study participants were equally concerned with both cervical cancer and genital warts. If given a choice between a vaccine that protected against 85% of cervical cancer only or one that protected against 75 % of cervical cancer and 100% of genital warts, participants chose the second by a margin of 5 to 1. Furthermore, 90% of women in the same study felt they should be vaccinated against HPV before the initiation of sexual activity (FIGURE 1). (3) Strong objections regarding this issue may arise, since studies have shown that immunization against some sexually transmitted infections (STIs) may lead to a decrease in responsible sexual behavior and an increase in the rate of high-risk sexual behaviors. (5,6) However, in a study by Kahn et al, most of the participants reported that after vaccination with an HPV vaccine, they would not feel safe engaging in high-risk sexual behaviors such as having multiple sex partners and having sex without using condoms. (7) This indicates that the increase in high-risk behaviors may not be significant. Also, HPV is usually considered a relatively minor infection in the STI hierarchy; therefore, it is not likely to drive decision making about high-risk sexual behavior. (8) Finally, the fear of increased high-risk sexual behavior that prompted proposals that give women open access to emergency contraception turned out to be unfounded. (9)

Participants in the study by Kahn et al (7) also reported beliefs that people important to them would support their decision to receive an HPV vaccine. Nineteen percent of participants indicated that members of their church or synagogue would approve of them getting the vaccine, and an additional 25% felt the leaders of their religious institutions would be neutral. This demonstrates the significant role religious institutions can play in health care decisions.

Participants in this study also felt that both women and men should receive the vaccine. (7) Additional studies investigating the beliefs of men regarding this issue are needed, since men are an important part of the transmission cycle. By vaccinating men and women, the effect of herd immunity may further decrease overall cancer rates, especially among unvaccinated women with vaccinated partners. In addition, some men will have sex with men, and it is not possible to identify this subset during early adolescence, when a preventive vaccine is most beneficial; a preventive HPV vaccine may particularly benefit this group.

Issues concerning parents of adolescents

The HPV vaccines currently in development are designed to decrease disease burden; therefore, patients should ideally be vaccinated prior to being exposed to the virus. In the United States, this means that boys and girls aged 9-15 years in early adolescence would be ideal candidates, since individuals in this age-group have typically not yet initiated sexual activity or have not had time to acquire many HPV types. However, for an adolescent of this age to be vaccinated, he or she must obtain parental permission and have parental support. Therefore, parental understanding of the benefits and support of their children may be pivotal in determining whether an adolescent receives the vaccination. Investigators analyzing the major issues concerning parents of adolescent girls and vaccination against HPV have identified important deciding factors. The results of an anonymous questionnaire administered to parents or guardians of adolescents (boys and girls aged 10-15 years) to assess their attitudes toward HPV vaccination and its health benefits demonstrated that attitudes toward vaccines in general were the best predictor of acceptance of an HPV vaccine among participants in this study. Parents who would allow their children to receive the vaccine were more likely to believe that vaccines are effective in preventing disease, feel that it is important for their children to receive all their vaccinations, to have no fear of vaccines, and believe that vaccines are generally helpful. Fifty-five percent reported that they were willing to have their children vaccinated, 23% declined the vaccine, and 22% were undecided. After receiving educational information regarding HPV-related diseases and the benefits of HPV vaccination, 20% who initially did not want the vaccine and 65% of the undecided parents and guardians changed their minds and wanted the vaccine. Seventy-five percent of parents agreed to allow their children to be vaccinated, 20% declined the vaccine, and 5% were undecided (FIGURE 2). (10) This and other studies suggest that although initial acceptance of an HPV vaccine is high, education significantly increases the number of parents who decide to allow the vaccination. (10,11) In addition, physician recommendation and/or the requirement of vaccination by school systems were also very important factors that motivate parents toward acceptance of an HPV vaccine (FIGURE 3). Importantly, of those parents or guardians who declined the vaccine for their children, the majority feared that their children would be more prone to having sex once vaccinated against HPV--a notion that may not be correct, as previously noted. Parental education has been shown to overcome obstacles to HPV vaccine acceptance.

Barriers to vaccination in general

Common barriers to immunization in general fall into 3 broad categories: problems of access to medical care, lack of knowledge about the vaccine or target disease, and fears about vaccine safety.(12) Many patients, especially the financially disadvantaged, have problems accessing medical care, as well as paying for preventive medical care that is not covered by commercial or public services. The cost of vaccination (and presumably lack of payment coverage) has been identified as a barrier to HPV vaccination specifically. (4) Many parents also have vague concerns about vaccinations. These fears are sometimes increased by antivaccine groups who frequently use the Internet to distribute antivaccine literature. Although early trials demonstrate a high degree of safety with HPV vaccines, the safety data produced by phase III trials will need to be clearly communicated to patients. Internet resources will probably be a valuable tool to dispel unsubstantiated fears and misinformation. Studies have shown that parents of incompletely immunized children are likely to believe (incorrectly) that vaccines are riskier for their children than nonimmunization. (12) This belief may be based on concerns about vaccine side effects, belief that their child is not at risk, or a belief that the disease being prevented is not serious. Once the HPV vaccines become available, the public will require education on the HPV-related diseases as well as on the vaccine itself.

Most parents support immunization for their children. (13) Some of the common misconceptions about vaccines include the belief that too many vaccines may weaken the immune system or that they may cause chronic diseases such as asthma, autism, diabetes mellitus, or multiple sclerosis. However, modern refined vaccines contain many fewer antigens than 2 decades ago, thus the relative risks for such problems are potentially decreasing. Any causal relationships between vaccines and autism, diabetes, multiple sclerosis, or other autoimmune disorders have not been demonstrated in well-controlled trials. Thimerosal, a preservative once widely used in vaccines, has been the target of speculation concerning adverse vaccine reactions. However, it is less commonly used today, and there is no plan to use it in HPV vaccines. Parents may believe that some lots of vaccine are particularly dangerous, or that vaccines are unnatural, and therefore prefer "natural" disease-produced immunity. It may be pointed out to these objectors that the HPV vaccines provide protection without a risk for cancer, unlike the natural course of HPV infection.

Some parents or adult medical decision makers may believe they can control their child's exposure or susceptibility to disease, have doubts about the reliability of vaccine information, or feel they can rely on herd immunity to protect their child. The latter group should be informed that this approach not only increases the risk of their own children acquiring the disease, but also increases the risk for others, since some, albeit very few, immunized individuals may fail to develop immunity to HPV. This argument also supports the use of the vaccine in young males. Parents may also overestimate the frequency of rare adverse reactions to vaccines or underestimate the frequency of disease-related risks. This could be particularly worrisome in relation to HPV-related disease, since cervical cancer is a relatively rare complication of HPV infection. Educational efforts need to address all of the benefits of HPV vaccines, including the potential decrease in cervical cancer incidence, fewer high-grade Pap results requiring a potentially stressful, disruptive, and painful work-up; and for a quadrivalent vaccine, the elimination of most or all cases of genital condyloma acuminata.

Other psychosocial issues concerning women

The diagnosis of an STI like HPV can be embarrassing for both men and women. This was clearly demonstrated in the study by Hoover et al, when they found that women did not appreciate being approached to discuss HPV when in the presence of a boyfriend or husband. (3) Infection with HPV can often cause fear, guilt, anxiety, and other types of psychosocial distress, so health care providers and clinicians must be sensitive to the concerns of their patients.

Typically, patients are less anxious and more comfortable about their diagnosis if they are educated about their condition and available treatment options. (14) A viable strategy is to partner with patients to maximize their involvement and include them in the decision-making process. Such patients are less likely to become anxious and regretful, regardless of the clinical outcome. Therefore, it may be helpful to produce materials that explain HPV-related diseases to patients, inform patients about how the diseases are managed, and highlight the patient's role in the decision-making process. (15) This implies that pediatric and adolescent health care providers will need to introduce the idea of HPV vaccination before the need to decide whether to get the vaccine. This allows for multiple opportunities for patients and parents to discuss the vaccine and become educated in a nonstressful environment. General recommendations for patient education include talking in simple everyday language, discussing the content of written materials with the patient, and providing materials that are culturally sensitive and appropriate to the educational level. (16)

Analysis of news media coverage of HPV has shown frequent inaccuracy, incompletion, and failure to emphasize the importance of the link between high-risk HPV types and cervical cancer, and the stories are often missing vital information regarding HPV prevention, transmission, and symptoms. (17) It is important for clinicians to provide accurate, salient, and understandable information regarding HPV directly to the patients and their parents or guardians. Incorporating mass media into public educational efforts is necessary, because women often use shared decision-making processes when solving medical problems.

Recommendations for patient education

Patient education is an essential facet of HPV vaccine acceptance. Only one third of the US population is actually aware of HPV, especially among high school and college-age females? Most students attending universities have heard of genital warts, yet between 28% and 67% do not know that they are caused by HPV. (18,19) Surprisingly, of those students who have heard of HPV, a small number do not know that it can be transmitted by skin-to-skin contact of external genitalia alone, regardless of whether condoms are used? (18) These same students are unaware of the link between HPV and cervical cancer and the fact that HPV infection is often asymptomatic. (1,20)

Insufficient knowledge of HPV infection can be overcome by proper patient education. This approach, as described by Whitney and colleagues, involves shared decision making and could potentially be beneficial. (21) In this approach, a clinician provides relevant and detailed information about HPV-related diseases and their prevention. In return, the patient conveys his or her feelings, beliefs, and worries regarding HPV, general knowledge of HPV, and personal preference for the information most interesting to the patient. (22,23)

Each patient is an individual; therefore, education should be tailored based on background, age, and literacy level. Studies have shown that literacy is a major obstacle to cancer prevention and treatment. (16,24) Hence, the manner in which a clinician communicates the content regarding HPV may be just as important as the information itself.

Patient education is pivotal to the acceptance of a vaccine for HPV-related diseases. Patients of different age-groups and social backgrounds have particular preferences regarding education; therefore, clinicians must consider what women want to know about HPV-related diseases and the attitudes of adolescent and adult women, as well as issues that may influence vaccine acceptance.

References

(1.) Kaiser Family Foundation. National Survey of Public Knowledge of HPV, the Human Papillomavirus. Available at: http://www.kff.org/womenshealth/upload/13385_1.pdf.

(2.) Anhang R, Wright TC Jr, Smock L, Goldie SJ. Women's desired information about human papillomavirus. Cancer. 2004;100:315-320.

(3.) Hoover DR, Carfioli B, Moench EA. Attitudes of adolescent/young adult women toward human papillomavirus vaccination and clinical trials. Health Care Women Int. 2000;21:375-391.

(4.) Zimet GD, Mays RM, Winston Y, Kee R, Dickes J, So L. Acceptability of human papillomavirus immunization. J Womens Health Gend Based Med. 2000;9:47-50.

(5.) Zimet GD, Mays RM, Fortenberry JD. Vaccines against sexually transmitted infections: promise and problems of the magic bullets for prevention and control. Sex Transm Dis. 2000;27:49-52.

(6.) Webb PM, Zimet GD, Mays R, Fortenberry JD. HIV immunization: acceptability and anticipated effects on sexual behavior among adolescents. J Adolesc Health. 1999;25:320-322.

(7.) Kahn JA, Rosenthal SL, Hamann T, Bernstein DI. Attitudes about human papillomavirus vaccine in young women. Int J STD AIDS. 2003;14:300-306.

(8.) Garnett GP, Waddell HC. Public health paradoxes and the epidemiological impact of an FIPV vaccine. J Clin Virol. 2000;19:101-111.

(9.) Raine TR, Harper CC, Rocca CH, et al. Direct access to emergency contraception through pharmacies and effect on unintended pregnancy and STIs: a randomized controlled trial, JAMA. 2005;293:54-62.

(10.) Davis K, Dickman ED, Ferris D, Dias JK. Human papillomavirus vaccine acceptability among parents of 10- to 15-year-old adolescents. Obstet Gynecol Surv. 2004;59:820-822.

(11.) Lazcano-Ponce E, Rivera L, Arillo-Santillan E, et al. Acceptability of a human papillomavirus (HPV) trial vaccine among mothers of adolescents in Cuernavaca, Mexico. Arch Med Res. 2001;32:243-247.

(12.) Burns IT, Zimmerman RK. Immunization barriers and solutions. J Fam Pract. 2005;54:S58-S62.

(13.) Kimmel SR, Wolfe RM. Communicating the benefits and risks of vaccines. J Fam Pract. 2005;54:S51-S57.

(14.) Llewellyn-Thomas HA. Patients' health-care decision making: a framework for descriptive and experimental investigations. Med Decis Making. 1995;15:101-106.

(15.) O'Connor AM, Stacey D, Entwistle V, et al. Decision aids for people facing health treatment or screening decisions. Cocbrane Database Syst Rev. 2003:CD001431.

(16.) Mayeaux EJ Jr, Murphy PW, Arnold C, Davis TC, Jackson RH, Sentell T. Improving patient education for patients with low literacy skills. Am Fam Physician. 1996;53:205-211

(17.) Anhang R, Sttyker JE, Wright TC Jr, Goldie SJ. News media coverage of human papillomavirus. Cancer. 2004;100:308-314.

(18.) Baer H, Allen S, Braun L. Knowledge of human papillomavirus infection among young adult men and women: implications for health education and research. J Community Health. 2000;25:67-78.

(19.) Ramirez JE, Ramos DM, Clayton L, Kanowitz S, Moscicki AB. Genital human papillomavirus infections: knowledge, perception of risk, and actual risk in a nonclinic population of young women. J Womens Health. 1997;6:113-121.

(20.) Yacobi E, Tennant C, Ferrante J, Pal N, Roetzheim R. University students' knowledge and awareness of HPV. Prey Med. 1999;28:535-541.

(21.) Whitney SN, McGuire AL, McCullough LB. A typology of shared decision making, informed consent, and simple consent. Ann Intern Med. 2004;140:54-59.

(22.) Braddock CH 3rd, Fihn SD, Levinson W, Jonsen AR, Pearlman RA. How doctors and patients discuss routine clinical decisions: informed decision making in the outpatient setting. J Gen Intern Med. 1997;12:339-345.

(23.) Charles C, Gafni A, Whelan T. Decision-making in the physician-patient encounter: revisiting the shared treatment decision-making model. Soc Sci Med. 1999;49:651-661.

(24.) Davis TC, Williams MV, Marin E, Parker RM. Glass J. Health literacy and cancer communication. CA Cancer J Clin. 2002;52:134-149.

Edward J. Mayeaux, Jr, MD, FAAP

Departments of Family Medicine, and Obstetrics and Gynecology

Louisiana State University Health Sciences Center Shreveport, LA
FIGURE 1

Attitudes of adolescent/young adult women toward HPV vaccination

                                       When women
                       HPV vaccine   should receive
Response (%)            preferred     HPV vaccine

Protect 85% Cervical      16.7
  Cancer
Protect 70% Cervical      83.3
  Cancer 100%
  Genital Warts
Doesn't Matter                            6.7
After Becoming                            5.0
  Sexually Active
Before Becoming                          88.3
  Sexually Active
Not, Strongly
  Disagree
No, Somewhat
  Disagree
Yes, Somewhat
  Agree
Yes, Stongly
  Agree
Extremely Unlikely
Somewhat Unlikely
Somewhat Likely
Extremely Likely

                            Men should    Would partici-
                            receive HPV   pant pay for
Response (%)                  vaccine      the vaccine

Protect 85% Cervical
  Cancer
Protect 70% Cervical
  Cancer 100%
  Genital Wartz
Doesn't Matter
After Becoming
  Sexually Active
Before Becoming
  Sexually Active
Not, Stongly                    1.7
  Disagree
No, Somewhat                    3.3
  Disagree
Yes, Somewhat                  26.7
  Agree
Yes, Strongly                  68.3
  Agree
Extremely Unlikely                              6.7
Somewhat Unlikely                              25.0
Somewhat Likely                                53.3
Extremely Likely                               15.0

Note: Table made from bar graph.

FIGURE 2

Impact of educational intervention
on decision of parents of adolescents
to receive an HPV vaccine *

Percent Reporting

                                  Did not want                 Wanted
                                  vaccine for                 vaccine
                                     child       Undecided   for child

Before Educational Intervention       23            22           55
After Educational Intervention        20             5           75

* Subjects were asked the following question: "Do you want your
child to receive the HPV vaccine?"

Note: Table made from bar graph.

FIGURE 3

Primary influence for HPV vaccination *

Response (%)

                     Yes   No   No response

Doctor                66   53        67        P =  .03
School Requirement    29   48        38        P =  .001
Friend                 1              2        P =  .38
Nurse                  5    4         2        P =  .41
Spouse                 4    3         4        P =  .89
Relative               5    3         4        P =  .78
Advertisement          2    3         3        P = 1.00

P < .001 * Question asked to parents and guardians: "Do you want your
child to receive the HPV vaccine?"

Note: Table made from bar graph.
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Title Annotation:human papillomavirus
Author:Mayeaux, Edward J., Jr.
Publication:Journal of Family Practice
Geographic Code:1USA
Date:Jul 15, 2005
Words:3926
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