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Acceptability of human papillomavirus vaccines among women older than 26 years
Vaccine 33 (2015) 1556–1561
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Acceptability of human papillomavirus vaccines among women older than 26 years Amanda F. Dempsey ∗ , Sarah E. Brewer, Jennifer Pyrzanowski, Carter Sevick, Sean T. O’leary Adult and Child Center for Outcomes Research and Dissemination Science (ACCORDS), University of Colorado Denver, Denver, CO, United States
a r t i c l e
i n f o
Article history: Received 6 November 2014 Received in revised form 5 February 2015 Accepted 6 February 2015 Available online 19 February 2015 Keywords: Human papillomavirus Vaccine
a b s t r a c t Objective: To examine older women’s (>26 years) acceptance of the human papillomavirus (HPV) vaccine, and factors associated with this outcome. Study design: A convenience sample of 872 women age 26–77 years were surveyed regarding the likelihood they would accept the HPV vaccine if offered to them by their provider, and factors associated with this outcome. Binomial regression, Chi square and MacNemar’s analyses were used to determine associations of this outcome with demographic, attitudinal, and experiential variables. Results: The response rate was 60.8%. Half the respondents indicated they would want the vaccine, even if they had to pay for it. In multivariable analyses, the only factor associated with wanting the vaccine was higher self-reported knowledge about HPV (risk ratio 1.43, 95% Confidence Interval 1.12, 1.83). A majority of participants also believed that older women in general would want the vaccine if it were covered by insurance. However, this perspective was significantly diminished if the vaccine had to be paid for out of pocket (97% vs. 22% for 26–45 year olds; 84% vs. 20% for 46–65 year olds, 60% vs. 8% for 66+ year olds, p < 0.001). Nearly all (93%) believed primary care physicians should routinely discuss the vaccine with older women. Conclusions: A high proportion of women over 26 would want the HPV vaccine if offered by their provider, even if they had to pay for it out of pocket. This suggests that if providers were to routinely offer the HPV vaccine to their older patients, many women would choose to get vaccinated. © 2015 Elsevier Ltd. All rights reserved.
1. Introduction For U.S. females the human papillomavirus (HPV) vaccine is licensed for ages 9–26 years. This upper age cut off corresponds to the age of women in the main clinical trials evaluating the vaccine’s efficacy [1–3]. Demonstrating clinical efficacy of the vaccine becomes more difficult as women age because there are fewer HPV-naïve women to evaluate, and fewer incident HPV-associated cervical abnormalities to assess as clinical trial endpoints. However, there are data to support the safety and usefulness of the vaccine among older women (defined here as women over the age of licensure (26 years) in the U.S.), with efficacy reported as high as 83.4% in some studies [4–6]. Some countries have already licensed the vaccine for women age 27 to 45 years [7,8]; however, in 2011 the
∗ Corresponding author at: ACCORDS Program, University of Colorado Denver, 13199 East Montview Boulevard, Suite 300, Aurora, CO 80045, United States. Tel.: +1 303 724 6679; fax: +1 303 724 1839. E-mail address: [email protected] (A.F. Dempsey). http://dx.doi.org/10.1016/j.vaccine.2015.02.018 0264-410X/© 2015 Elsevier Ltd. All rights reserved.
U.S. FDA decided not to license the vaccine for this age group, citing a lack of effectiveness in preventing cervical cancer [9]. Studies in the early 2000s, many of which occurred before the vaccine was licensed, found broad acceptability for the HPV vaccine among women over 26, but also identified barriers such as insurance coverage and costs for this age group [10]. Little research has been done in more recent years on the attitudes about HPV vaccines among women older than 26 years. Such research is important because older women are still significantly impacted by HPV-related diseases, and can also serve as a reservoir for spreading the infection to others [11]. In the U.S. insurance coverage for vaccines generally mirrors licensure specifications [12]. Thus, because HPV vaccines are only licensed up to age 26, women older than this who want the vaccine would likely have to pay for it out of pocket. Out of pocket cost has been cited as a barrier to getting the vaccine among those lacking insurance coverage, regardless of age [13]. Given this, medical practitioners are much less likely to discuss the HPV vaccine with their older patients and potentially miss offering it to women who may benefit from the vaccine and be willing to pay for it [14].
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Understanding whether women over the age of 26 would want to be vaccinated against HPV, even if they had to pay out of pocket, is important as this knowledge may reveal a population that would benefit from the vaccine but for whom the vaccine is not currently being routinely discussed or offered. The goals of this study therefore were to investigate older women’s attitudes about HPV vaccines for themselves and for other women over the age of 26, how these attitudes may be influenced by whether a woman would have to pay out of pocket for the vaccine, and whether older women think that primary care providers in general should routinely discuss the vaccine with their older female patients.
2. Materials and methods The study population consisted of a convenience sample of 872 women attending one of nine private obstetrics and gynecology (ob-gyn) practices in the central Colorado area (6 urban, 3 rural). Women were eligible for the study if they had agreed to be contacted for a follow-up survey after completing a previous paper-based survey on a different topic, provided a working email address, were over the age of 26 years, and could complete the survey in English. A web-based survey administered via REDCap (Research Electronic Data Capture) [15] was provided to women at their contact email address beginning in February 2014. Women who had not completed the survey within one week of the initial email received up to 8 additional reminder emails and one automated phone call over a period of 9 weeks. A $5 incentive was provided to women completing the survey. All study activities were approved by Colorado’s Multiple Institutional Review Board. Before answering survey questions, participants were provided with a brief synopsis of HPV infection and vaccination. This paragraph described the likelihood of getting HPV and its potential clinical sequelae, the efficacy of the vaccine in younger women, and a suggestion that the vaccine may also be effective for older women (“Based on what is known, it is expected that the vaccine would potentially be beneficial to older women – especially those who have had only a small number of lifetime sexual partners and thus less exposure to the virus”). It also explained that vaccination for those over the age of 26 years would not likely be covered by insurance (“Because of the age restrictions for insurance coverage, if a woman older than 26 gets the vaccine, she would have to pay for the vaccine herself. The vaccine costs about $150/dose. Three doses of the vaccine are needed for protection so the patient’s total cost would be about $450”). A full version of the survey is available upon request. The main outcome assessed was a woman’s desire to get the HPV vaccine for herself if the vaccine was recommended by her ob-gyn, which was asked specifically among women who indicated they had not received any prior doses of the vaccine (94% [498/527] of respondents). This was measured using a 4-point Likert scale (“definitely would want” to “definitely would not want” the vaccine) in response to the question “Given the information provided, how much would you personally want to receive the HPV vaccine if your OB/GYN provider had it available and recommended it for you?” This response was later dichotomized to definitely/probably would want vs. definitely/probably would not want given the data’s distribution, and because the ultimate decision to receive a vaccine is a yes or no decision. A variety of secondary outcomes among all respondents (i.e. those with and without prior HPV vaccine doses, n = 527) were also assessed. Participants’ perceptions of other women wanting the vaccine were measured using the same 4-point Likert scale, and were assessed for three different hypothetical age categories (27–45 years, 46–65 years, and 66+ years), with and without hypothetical insurance coverage for the vaccine. Participants were also queried about how much they felt they knew about HPV (nothing/a
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little vs. some vs. a lot), whether they had ever discussed the HPV vaccine with their primary care provider, whether primary care providers in general should “routinely talk about the HPV vaccine with their female patients who are over age 26” (4-point Likert from strongly agree to strongly disagree), a variety of reasons why they would or would not want the HPV vaccines for themselves, and whether “they or anyone close to them” had experience with a variety of HPV-related diseases (defined in this study as “personal experience with HPV”). A 7-item series of true/false questions about the virus was used to generate a HPV knowledge ‘score’ for each participant that was later divided into three HPV knowledge categories (low – <58% correct, moderate – 58–83% correct and high – >83% correct) based on the distribution of correct answers. Demographic characteristics assessed included age of the participant (categorized later as 26–34, 35–44, 45–54, and 55+ years), education level (later consolidated to some high school/high school grad vs. some college/college grad vs. advanced degree), household income (later consolidated to <$50 k vs. $50 k–$99,999 k vs. $100 k+), race (later dichotomized to white vs. other), insurance type (later consolidated to public vs. private vs. other), whether they were currently the parent of an adolescent son or daughter, whether or not they had a chronic health condition (defined as any health condition lasting longer than 3 months), and what type of medical provider they saw as their primary care doctor (later categorized as ob-gyn vs. internal/family medicine vs. other). Descriptive statistics were generated for all survey questions. The association between the various outcome measures and predictor variables was assessed using Chi-square, Fisher’s exact or MacNemar’s tests as appropriate. Univariable and multivariable log binomial regression analyses were used to identify independent predictors of participants wanting the HPV vaccine for themselves. The multivariable model included items that were found to be possibly significantly associated (p ≤ 0.1) with this outcome in univariable analyses plus race, age, education, and insurance type, as these have been shown in studies of younger women to be important predictors of HPV vaccination [16,17]. Given the high prevalence of the main outcome, risk ratios (RR) were chosen as the reporting measure rather than OR. Trends of vaccine acceptance across the three age categories for hypothetical older women were assessed using generalized estimating equations to account for repeated measures among participants, and included only those participants who provided an answer for all three hypothetical age categories. All analyses were performed in SAS 9.2 (Cary, NC).
3. Results Less than 1% (5/872) of our survey sample was unable to be reached via email (i.e. email bounce backs). Of those reached, 527 responded to the survey for a response rate of 61%. There were 29 women (5.6% of the total sample) who indicated they had already received the HPV vaccine series, and were therefore excluded from analyses regarding wanting the vaccine for themselves. There was no difference between responders and non-responders in age, pregnancy status or whether they had received the HPV vaccine previously. Table 1 shows the demographic characteristics of 527 respondents. Most women had heard of HPV previously (Table 2). Only 17% of women felt they knew “a lot” about HPV. Consistent with previous studies [11,18–20] a high proportion (76%) of women or “someone close to them” had experienced HPV infection and related sequelae (Table 2). Half of the unvaccinated women in our study indicated they would “probably” or “definitely” get the vaccine if it their provider had it available and recommended it for them. Prevention of cervical cancer was the most common reason endorsed by women
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Table 1 Participant demographics (n = 527).d Characteristic
% (n)
Age 26–34 35–44 45–54 55–77 Education Some high school/high school grad Some college/college grad Advanced degree Race White Other Household income <$50 k $50–99,999 k $100 k+ Prefer not to answer Health Insurance Public Private No insurance/other Parent of an adolescent age 11–17 Has adolescent sona Has adolescent daughtera Has chronic health conditionb Primary care physicianc Ob-gyn Internist/family medicine Other
30% (160) 30% (157) 23% (120) 17% (89) 10% (50) 61% (314) 29% (152) 89% (449) 11% (57) 15% (76) 39% (200) 36% (185) 10% (51) 3% (16) 90% (465) 7% (36) 23% (118) 13% (66) 15% (79) 32% (163) 24% (122) 70% (360) 7% (34)
a Participants could have both sons and daughters who are adolescents, thus summation of these two groups is greater than “parent of adolescent age 11–17.” b Defined as a positive response to the question “Do you have a health condition or health problem that has lasted longer than 3 months?” c Percentages do not add to 100% due to rounding. d Missing values were excluded from the denominator if >10% of the survey sample.
wanting the vaccine (86%, n = 212) followed by “doing what the ob-gyn provider recommends” (42%, n = 103). Only 7% (n = 17) of women endorsed the statement “I think I might be at risk for HPV” as a reason for wanting the vaccine. Among women who did not
want the vaccine, 41% (n = 100) indicated the reason for their decision was because they thought the vaccine would be too expensive, and 39% (n = 95) indicated that they did not think they were at risk for HPV. Eleven percent (n = 26) indicated that they “do not generally get vaccines” as a reason for not wanting the HPV vaccine. In univariable analyses (Table 2) higher self-perceived knowledge about HPV and personal experience with a positive HPV test, genital warts, and cervical cancer were significantly associated with wanting the HPV vaccine for oneself. In multivariable analyses (Table 3) only self-perceived knowledge about HPV remained statistically associated with this outcome when controlling for other variables. Participants were queried whether they believed older women in general would want the vaccine. Separate questions were asked for three age categories of hypothetical women (27–45, 46–65 and 66+), and with or without hypothetical insurance coverage for the vaccine. As shown in Table 4, for each hypothetical age category, a significantly higher proportion of women were believed to want the vaccine if it was covered by insurance. As the age of the hypothetical women increased, there was a statistically significant trend for a decreased proportion of women believed to want the vaccine (Table 4). However, it was notable that even at the highest hypothetical age category being considered (66+ years), a majority of participants (60%) still believed that these oldest women would want the vaccine if covered by insurance. The only consistent predictor of believing other women would want the vaccine was wanting the vaccine for oneself. Overall, 36% of women had discussed the HPV vaccine previously with their primary care provider. In univariable analyses, discussion with the provider was significantly associated with having higher self-reported knowledge about HPV (p < 0.0001) but not the actual knowledge score. It was also associated with being the parent of an adolescent (p = 0.0004), having an ob-gyn as the primary care provider (p = 0.0042), not having a chronic health condition (p = 0.0078), younger age (p < 0.0001), higher education (p = 0.0331), and personal experience with HPV, including known exposure to partner with HPV (p = 0.0014), previous positive HPV test (p = .0005), and having experienced an HPV-related problem previously (p = 0.0036). Prior discussion of HPV vaccine with the
Table 2 Older women’s knowledge and experience with HPV, n = 461.d Characteristic
Sample overall % (n)
Likelihood of getting the HPV vaccine if offered Probably/definitely would get % (n)
Probably not/definitely not would get % (n)
p-Value
Ever heard of HPV before study
94% (461)
94% (231)
94% (230)
Self-report of amount known about HPV Nothing/a little Some A lot
36% (176) 49% (240) 15% (73)
34% (82) 47% (116) 19% (47)
39% (94) 51% (124) 11% (26)
Knowledge scorea Low Moderate High
38% (188) 28% (140) 33% (165)
38% (94) 29% (72) 33% (81)
38% (94) 28% (68) 34% (84)
Abnormal Pap smearb
71% (348)
72% (177)
70% (171)
0.60
Positive HPV testb
26% (127)
30% (73)
22% (54)
0.05
Genital wartsb
21% (103)
26% (63)
16% (40)
0.0116
14% (68)
17% (42)
11% (26)
0.0383
9% (46)
10% (25)
9% (21)
0.55
76% (375)
79% (196)
73% (179)
0.09
0.0284
0.92
b
Cervical cancer
Known exposure to partner with HPVb c
Ever experienced HPV a
>0.99
Categorized using the mean number of correct responses to 7 true/false knowledge questions. b Asked using the stem “Have you or anyone close to you ever had. . .”. c A composite variable defined as positive response to ≥1 HPV related health condition listed above. d Restricted to the subset of women who indicated they had not received prior HPV vaccine doses and had non-missing data. Bold lettering denotes statistically significant results.
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Table 3 Univariable and multivariable associations of definitely or probably wanting the HPV vaccine for oneself if available, n = 461. Variable
Multivariableb
Univariable RR (95% CI)
Age 26–34 35–44 45–54 55–87 Education Some high school/high school grad Some college/college grad Advanced degree Race White Other Household income <$50 k $50–99,999 k $100 k+ Prefer not to answer Health Insurance Public/no insurance/othera Private Parent of an adolescent age 11–17 Has adolescent son Has adolescent daughter Has chronic health condition Primary care physician Ob-gyn Internist/family medicine Other Ever heard of HPV before study Self-report of amount known about HPV Nothing/a little Some A lot Knowledge score Lo Moderate High Ever experienced HPV
p-Value
RR (95% CI)
0.9881
p-Value 0.9765
Ref. 1.03 (0.82, 1.30) 1.00 (0.78, 1.28) 1.00 (0.76, 1.31)
Ref. 1.04 (0.81, 1.32) 1.02 (0.79, 1.32) 1.06 (0.80, 1.40) 0.9206
0.8732
Ref. 0.95 (0.71, 1.27) 0.98 (0.72, 1.34)
Ref. 0.92 (0.69, 1.23) 0.94 (0.68, 1.29) 0.3121
0.1052
Ref. 1.15 (0.89, 1.50)
Ref. 1.27 (0.97, 1.67) –
0.9790
–
Ref. 0.99 (0.75, 1.31) 1.02 (0.77, 1.35) 0.96 (0.66, 1.40) 0.41 Ref. 0.94 (0.71, 1.24) 0.99 (0.81, 1.22) 0.81 (0.60, 1.09) 1.09 (0.87, 1.36) 1.04 (0.87, 1.26)
0.66 Ref. 0.94 (0.71–1.24) 0.97 (0.78, 1.21) –
0.9601 0.1329 0.4828 0.6525 0.4972
Ref. 1.13 (0.90, 1.42) 1.02 (0.67, 1.55) 1.00 (0.67, 1.55)
– –
>0.99 0.0272
–
Ref. 1.04 (0.84, 1.27) 1.40 (1.10, 1.74) Ref. 1.03 (0.83, 1.27) 0.98 (0.79, 1.21) 1.21 (0.96, 1.52)
0.7796 – – – –
– 0.0155
0.92
Ref. 1.03 (0.83, 1.27) 1.43 (1.12, 1.83) –
–
0.0861
1.17 (0.93, 1.48)
0.1675
a
Because of small sample size, “other” insurance was combined with “public” for the analysis. b The model includes only the variables with values listed. Bolded items indicate statistical significance.
provider was not associated with an increased likelihood of wanting the HPV vaccine for oneself. Almost all of the women surveyed (93%) believed that primary care physicians should discuss the HPV vaccine routinely with older women in general. The only factors that were associated with this outcome statistically were personally wanting the HPV vaccine for oneself (p < 0.0001), and having an ob-gyn as the primary care provider (p = 0.0059). 4. Comment In this study of women aged 26–77, half of the participants without prior HPV vaccination indicated they would probably or definitely want the HPV vaccine for themselves in the coming year
if their ob-gyn provider had it available and recommended it for them, even if they had to pay out of pocket for it. Wanting the vaccine for oneself was more prevalent among women who perceived they had a high level of knowledge about HPV, and among women who had prior experience with an HPV-related health condition in themselves or someone close to them. A majority of participants also believed that other older women would want the HPV vaccine if it were covered by insurance. However, the perceived likelihood of other older women wanting the vaccine was significantly less if women had to pay for the vaccine out of pocket. Nearly all women believed that primary care physicians in general should discuss the HPV vaccine routinely with women over age 26 years. In our study there was surprisingly little variation by demographic characteristics in the proportion of women wanting the
Table 4 Participants perceptions of other women wanting the HPV vaccine, by age and insurance, n = 611. Age category of hypothetical older women
27–45 46–65 66+ Trend statistic by agea a
Proportion of participants who perceive other women in general would “definitely” or “probably” want the HPV vaccine (n) If covered by insurance % (n)
If had to pay out of pocket % (n)
97% (496) 84% (435) 60% (303) <0.001
22% (115) 20% (103) 8% (40) <0.001
Analysis limited to those who answered for all three age groups assessed (n = 506 for “covered by insurance”, n = 512 for “pay out of pocket”).
p-Value
<0.001 <0.001 <0.001
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vaccine for themselves, or in the proportion believing that other older women would want the vaccine. The only exceptions to this were age and insurance. The proportion of respondents who believed that other older women would want the vaccine decreased with increasing age of the hypothetical women being considered, and was also markedly lower for all hypothetical age categories if there were no insurance coverage for the vaccine. However, neither age nor insurance status was related to whether a woman wanted the vaccine for herself. The majority of women in our study were insured, with relatively high education and income. Thus one hypothesis to explain this dichotomy in results is that women in our study did not perceive cost as a personal barrier to vaccination, but believed it could be a barrier to other women. To our knowledge there are only a small number of other studies that have examined attitudes about HPV vaccines among older women, and most occurred prior to or shortly after the vaccine’s licensure. In a study by Weiss et al. [21], which was performed in 2007 and included 451 women age 27–45 years, 71% of women surveyed indicated they would be likely or extremely likely to get the vaccine if it were offered in the future. Kahn et al. found that among nurses who were mothers of young women ages 9–18 about 48% would get the vaccine if it were recommended for them [22]. It is unclear whether in these two studies the potential cost of the vaccine was described. If not, this could explain why acceptability of the vaccine was higher in the Weiss study than in ours, where only 50% of women indicated the definitely or probably would want the vaccine if offered in the future. Our results are in keeping, however, with other studies on older women’s attitudes about HPV vaccines by Kahn et al. [22] and Ferris et al. [23,24], in which it was it was reported in 2006 that ∼50% of older women would want to get the HPV vaccine. Reasons for wanting or not wanting the vaccine were similar between both of these studies and our study. Other studies found similarly high acceptability among women 27 to 55, but each also report that cost was a potentially significant barrier to vaccination among this population and was associated with decrease acceptability and likelihood to vaccinate against HPV [25–27]. Current licensure by the FDA means that women over 26 in the U.S. who choose to receive the HPV vaccine would do so off-label, requiring out-of-pocket costs and likely limiting access to women with adequate financial resources. When the vaccine is covered by public and private insurance, vaccination is one of the best ways to reduce certain health disparities. However, this may not feasible for HPV vaccination of women over age 26. In the Ferris study, older women were less likely to endorse wanting to get the vaccine for themselves than younger women. This contrasts with our finding of no association between participant age and wanting the vaccine for oneself. One hypothesis to explain this difference is that our study was performed several years after the Ferris study, during which time public knowledge and awareness about HPV infection and vaccination has risen substantially. Heightened awareness among older women about the burden of HPV in their age group, plus increased public recognition that HPV infection is nearly ubiquitous among the sexually active population, could explain why in our study age appears to no longer be associated with wanting the vaccine. Physician recommendation has been shown to be one of the most consistent predictors of HPV vaccine utilization [28,29]. In our study, participants overwhelmingly believed that the vaccine should be routinely discussed by primary care providers with women over the age of 26. This finding, combined with the suggestion by our results that many women would be willing to pay out of pocket for the vaccine, implies that there may be substantial missed opportunities for HPV prevention among older women. Gynecologists may be in a unique position to enhance the health of women in this regard as they are not only keenly aware of the
potential health effects from HPV infection, but also are the primary care physician for a substantial proportion of mid-adult women, including 24% of the women in our study [30]. Prior research suggests that among medical specialties that serve as primary care providers, vaccines are less likely to be given to patients by gynecologists when compared to family medicine or internal medicine providers [31,32]. However, this is likely to change over time as more vaccines are recommended for pregnant women, allowing ob-gyns to become more experienced at immunization delivery. Moreover, medical organizations have recently identified improving immunization delivery as a priority area for ob-gyns nationally [33]. The question of whether ob-gyn providers should discuss and offer the HPV vaccine to women over the age of 26 is ultimately a balancing act of practice efficiency and maximum vaccine coverage and prevention of the sequelae of HPV infection. While some populations of women, especially those with the means to pay out-of-pocket for the vaccine, may benefit more from a practice of offering the vaccine off-label, practices should also take into account a women’s right to opt for vaccination. Since most women are naïve to at least some of the strains of HPV that vaccines protect against, most women would benefit to some extent from HPV vaccination. Providers and patients should consider discussing the costs and benefits of vaccination with women older than 26 so that each woman can make the right choice about HPV vaccination for themselves. Our study results should be interpreted with certain limitations in mind. First, our study took place within a discrete geographical area, and the study sample was relatively well educated, wealthy, and with little racial or ethnic diversity. Our study’s findings therefore cannot be generalized to other populations, particularly women who are at highest risk for HPV infection and its sequelae such as African Americans and those with lower incomes [34]. In addition, our main outcome measure was hypothetical acceptance of an HPV vaccine for oneself, which may or may not accurately reflect what a woman would do if actually given the opportunity to be vaccinated. In conclusion, in this study of 26–77 year old women, a high proportion (∼50%) would want to be vaccinated against HPV, even if they had to pay for it out of pocket. There was little variability by demographic characteristics among women wanting the vaccine for themselves, suggesting a broad acceptance of this vaccine among older women, and potentially among diverse populations. Though the vaccine is not currently licensed in the U.S. for women over the age of 26, older women still experience a substantial burden of HPV-related diseases and are frequently naïve to at least one HPV strain covered by the vaccine. Our study suggests that if providers were to offer the vaccine to their older patients as part of routine well woman care, many women would choose to get vaccinated. Funding source This work was funded by the Centers for Disease Control and Prevention (5U01-IP000501-03). The opinions expressed in this manuscript do not necessarily represent those of the funding agency. Survey administration through REDCap was supported by NIH/NCRR Colorado CTSI Grant (UL1 TR000154). Conflicts of interest Amanda Dempsey serves on Advisory boards for Merck and Pfizer. These companies played no role in this research study. Dr. Dempsey does not received research support from either company. All other authors have no conflicts of interest to declare.
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Condensation More than 50% of women surveyed age >26 years would want the HPV vaccine, even if they had to pay for it. References [1] The Future II Study Group. Prophylactic efficacy of a quadrivalent human papillomavirus (HPV) vaccine in women with virological evidence of HPV infection. J Infect Dis 2007;196(10):1438–46. [2] Harper DM, Franco EL, Wheeler C, Ferris DG, Jenkins D, et al. Efficacy of a bivalent L1 virus-like particle vaccine in prevention of infection with human papillomavirus types 16 and 18 in young women: a randomised controlled trial. Lancet 2004;364:1757–65. [3] Villa LL, Costa RL, Petta CA, Andrade RP, Paavonen J, et al. High sustained efficacy of a prophylactic quadrivalent human papillomavirus types 6/11/16/18 L1 virus-like particle vaccine through 5 years of follow-up. Br J Cancer 2006;95:1459–66. [4] Schwarz TF, Spaczynski M, Schneider A, Wysocki J, Galaj A, et al. Persistence of immune response to HPV-16/18 AS04-adjuvanted cervical cancer vaccine in women aged 15–55 years. Hum Vaccin 2011;7:958–65. [5] Schiller JT, Castellsague X, Garland SM. A review of clinical trials of human papillomavirus prophylactic vaccines. Vaccine 2012;30(5):F123–38. [6] Castellsague X, Munoz N, Pitisuttithum P, Ferris D, Monsonego J, et al. End-ofstudy safety, immunogenicity, and efficacy of quadrivalent HPV (types 6, 11, 16, 18) recombinant vaccine in adult women 24–45 years of age. Br J Cancer 2011;105:28–37. [7] Public Health Agency of Canada. Recommended immunization schedule, adults, not previously immunized; 2014. [8] Mazza D, Petrovic K, Grech C, Harris N. HPV vaccination in women aged 27 to 45 years: what do general practitioners think? BMC Womens Health 2014;14:91. [9] Vousden KH, Farrell PJ. Viruses and human cancer. Br Med Bull 1994;50:560–81. [10] Black LL, Zimet GD, Short MB, Sturm L, Rosenthal SL. Literature review of human papillomavirus vaccine acceptability among women over 26 years. Vaccine 2009;27:1668–73. [11] Dunne EF, Unger ER, Sternberg M, McQuillan G, Swan DC, et al. Prevalence of HPV infection among females in the United States. JAMA 2007;297:813–9. [12] Dempsey AF, Davis MM. Overcoming barriers to adherence to HPV vaccination recommendations. Am J Manag Care 2006;12:S484–91. [13] Small SL, Sampselle CM, Martyn KK, Dempsey AF. Modifiable influences on female HPV vaccine uptake at the clinic encounter level: a literature review. J Am Assoc Nurse Pract 2014;26(9):519–25. [14] Wong KY, Do YK. Are there socioeconomic disparities in women having discussions on human papillomavirus vaccine with health care providers? BMC Womens Health 2012;12:33. [15] Harris P, Taylor R, Thielke R, Payne J, Gonzalez N, Conde JG. Research electronic data capture (REDCap) – a metadata-driven methodology and workflow process for providing tranlsational research informatics support. J Biomed Inform 2009;42:377–81.
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[16] Kester LM, Zimet GD, Fortenberry JD, Kahn JA, Shew ML. A national study of HPV vaccination of adolescent girls: rates, predictors, and reasons for nonvaccination. Matern Child Health J 2013;17:879–85. [17] Gowda C, Dong S, Potter RC, Dombkowski KJ, Dempsey AF. A population-level assessment of factors associated with uptake of adolescent-targeted vaccines in Michigan. J Adolesc Health 2013;53:498–505. [18] Baseman JG, Koutsky LA. The epidemiology of human papillomavirus infections. J Clin Virol 2005;32(1):S16–24. [19] Markowitz LE, Dunne EF, Saraiya M, Lawson HW, Chesson H, et al. Quadrivalent human papillomavirus vaccine: recommendations of the advisory committee on immunization practices (ACIP). MMWR Recomm Rep 2007;56:1–24. [20] Markowitz LE, Sternberg M, Dunne EF, McQuillan G, Unger ER. Seroprevalence of human papillomavirus types 6, 11, 16, and 18 in the United States: national health and nutrition examination survey 2003–2004. J Infect Dis 2009;200:1059–67. [21] Weiss TW, Rosenthal SL, Zimet GD. Attitudes toward HPV vaccination among women aged 27 to 45. ISRN Obstet Gynecol 2011;2011:670318. [22] Kahn JA, Ding L, Huang B, Zimet GD, Rosenthal SL, et al. Mothers’ intention for their daughters and themselves to receive the human papillomavirus vaccine: a national study of nurses. Pediatrics 2009;123:1439–45. [23] Ferris DG, Waller JL, Owen A, Smith J. Midadult women’s attitudes about receiving the prophylactic human papillomavirus vaccine. J Low Genit Tract Dis 2007;11:166–72. [24] Ferris DG, Waller JL, Owen A, Smith J. HPV vaccine acceptance among mid-adult women. J Am Board Fam Med 2008;21:31–7. [25] Liau A, Stupiansky NW, Rosenthal SL, Zimet GD. Health beliefs and vaccine costs regarding human papillomavirus (HPV) vaccination among a U.S. national sample of adult women. Prev Med 2012;54:277–9. [26] Stupiansky NW, Rosenthal SL, Wiehe SE, Zimet GD. Human papillomavirus vaccine acceptability among a national sample of adult women in the USA. Sex Health 2010;7:304–9. [27] Short MB, Rosenthal SL, Sturm L, Black L, Loza M, et al. Adult women’s attitudes toward the HPV vaccine. J Womens Health (Larchmt) 2010;19:1305–11. [28] Gargano LM, Herbert NL, Painter JE, Sales JM, Morfaw C, Rask K, et al. Impact of a physician recommendation and parental immunization attitudes on receipt or intention to receive adolescent vaccines. Hum Vaccin Immunother 2013;9. [29] Rosenthal SL, Weiss TW, Zimet GD, Ma L, Good MB, et al. Predictors of HPV vaccine uptake among women aged 19–26: importance of a physician’s recommendation. Vaccine 2011;29:890–5. [30] Rayburn WF, Petterson SM, Bazemore A. Preferences of sites for office-based care by reproductive-aged women. Obstet Gynecol 2014;123(1):88S. [31] Dempsey A, Cohn L, Dalton VA, Ruffin M. Patient and clinic factors associated with adolescent human papillomavirus vaccine utilization within a universitybased health system. Vaccine 2010;28:989–95. [32] Dempsey A, Cohn L, Dalton V, Ruffin M. Worsening disparities in HPV vaccine utilization among 19–26 year old women. Vaccine 2011;29:528–34. [33] ACOG. ACOG committee opinion no. 558: integrating immunizations into practice. Obstet Gynecol 2013;121:897–903. [34] Rositch AF, Nowak RG, Gravitt PE. Increased age and race-specific incidence of cervical cancer after correction for hysterectomy prevalence in the United States from 2000 to 2009. Cancer 2014;120(13):2032–8.
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Acceptability of human papillomavirus vaccines among women older than 26 years Amanda F. Dempsey ∗ , Sarah E. Brewer, Jennifer Pyrzanowski, Carter Sevick, Sean T. O’leary Adult and Child Center for Outcomes Research and Dissemination Science (ACCORDS), University of Colorado Denver, Denver, CO, United States
a r t i c l e
i n f o
Article history: Received 6 November 2014 Received in revised form 5 February 2015 Accepted 6 February 2015 Available online 19 February 2015 Keywords: Human papillomavirus Vaccine
a b s t r a c t Objective: To examine older women’s (>26 years) acceptance of the human papillomavirus (HPV) vaccine, and factors associated with this outcome. Study design: A convenience sample of 872 women age 26–77 years were surveyed regarding the likelihood they would accept the HPV vaccine if offered to them by their provider, and factors associated with this outcome. Binomial regression, Chi square and MacNemar’s analyses were used to determine associations of this outcome with demographic, attitudinal, and experiential variables. Results: The response rate was 60.8%. Half the respondents indicated they would want the vaccine, even if they had to pay for it. In multivariable analyses, the only factor associated with wanting the vaccine was higher self-reported knowledge about HPV (risk ratio 1.43, 95% Confidence Interval 1.12, 1.83). A majority of participants also believed that older women in general would want the vaccine if it were covered by insurance. However, this perspective was significantly diminished if the vaccine had to be paid for out of pocket (97% vs. 22% for 26–45 year olds; 84% vs. 20% for 46–65 year olds, 60% vs. 8% for 66+ year olds, p < 0.001). Nearly all (93%) believed primary care physicians should routinely discuss the vaccine with older women. Conclusions: A high proportion of women over 26 would want the HPV vaccine if offered by their provider, even if they had to pay for it out of pocket. This suggests that if providers were to routinely offer the HPV vaccine to their older patients, many women would choose to get vaccinated. © 2015 Elsevier Ltd. All rights reserved.
1. Introduction For U.S. females the human papillomavirus (HPV) vaccine is licensed for ages 9–26 years. This upper age cut off corresponds to the age of women in the main clinical trials evaluating the vaccine’s efficacy [1–3]. Demonstrating clinical efficacy of the vaccine becomes more difficult as women age because there are fewer HPV-naïve women to evaluate, and fewer incident HPV-associated cervical abnormalities to assess as clinical trial endpoints. However, there are data to support the safety and usefulness of the vaccine among older women (defined here as women over the age of licensure (26 years) in the U.S.), with efficacy reported as high as 83.4% in some studies [4–6]. Some countries have already licensed the vaccine for women age 27 to 45 years [7,8]; however, in 2011 the
∗ Corresponding author at: ACCORDS Program, University of Colorado Denver, 13199 East Montview Boulevard, Suite 300, Aurora, CO 80045, United States. Tel.: +1 303 724 6679; fax: +1 303 724 1839. E-mail address: [email protected] (A.F. Dempsey). http://dx.doi.org/10.1016/j.vaccine.2015.02.018 0264-410X/© 2015 Elsevier Ltd. All rights reserved.
U.S. FDA decided not to license the vaccine for this age group, citing a lack of effectiveness in preventing cervical cancer [9]. Studies in the early 2000s, many of which occurred before the vaccine was licensed, found broad acceptability for the HPV vaccine among women over 26, but also identified barriers such as insurance coverage and costs for this age group [10]. Little research has been done in more recent years on the attitudes about HPV vaccines among women older than 26 years. Such research is important because older women are still significantly impacted by HPV-related diseases, and can also serve as a reservoir for spreading the infection to others [11]. In the U.S. insurance coverage for vaccines generally mirrors licensure specifications [12]. Thus, because HPV vaccines are only licensed up to age 26, women older than this who want the vaccine would likely have to pay for it out of pocket. Out of pocket cost has been cited as a barrier to getting the vaccine among those lacking insurance coverage, regardless of age [13]. Given this, medical practitioners are much less likely to discuss the HPV vaccine with their older patients and potentially miss offering it to women who may benefit from the vaccine and be willing to pay for it [14].
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Understanding whether women over the age of 26 would want to be vaccinated against HPV, even if they had to pay out of pocket, is important as this knowledge may reveal a population that would benefit from the vaccine but for whom the vaccine is not currently being routinely discussed or offered. The goals of this study therefore were to investigate older women’s attitudes about HPV vaccines for themselves and for other women over the age of 26, how these attitudes may be influenced by whether a woman would have to pay out of pocket for the vaccine, and whether older women think that primary care providers in general should routinely discuss the vaccine with their older female patients.
2. Materials and methods The study population consisted of a convenience sample of 872 women attending one of nine private obstetrics and gynecology (ob-gyn) practices in the central Colorado area (6 urban, 3 rural). Women were eligible for the study if they had agreed to be contacted for a follow-up survey after completing a previous paper-based survey on a different topic, provided a working email address, were over the age of 26 years, and could complete the survey in English. A web-based survey administered via REDCap (Research Electronic Data Capture) [15] was provided to women at their contact email address beginning in February 2014. Women who had not completed the survey within one week of the initial email received up to 8 additional reminder emails and one automated phone call over a period of 9 weeks. A $5 incentive was provided to women completing the survey. All study activities were approved by Colorado’s Multiple Institutional Review Board. Before answering survey questions, participants were provided with a brief synopsis of HPV infection and vaccination. This paragraph described the likelihood of getting HPV and its potential clinical sequelae, the efficacy of the vaccine in younger women, and a suggestion that the vaccine may also be effective for older women (“Based on what is known, it is expected that the vaccine would potentially be beneficial to older women – especially those who have had only a small number of lifetime sexual partners and thus less exposure to the virus”). It also explained that vaccination for those over the age of 26 years would not likely be covered by insurance (“Because of the age restrictions for insurance coverage, if a woman older than 26 gets the vaccine, she would have to pay for the vaccine herself. The vaccine costs about $150/dose. Three doses of the vaccine are needed for protection so the patient’s total cost would be about $450”). A full version of the survey is available upon request. The main outcome assessed was a woman’s desire to get the HPV vaccine for herself if the vaccine was recommended by her ob-gyn, which was asked specifically among women who indicated they had not received any prior doses of the vaccine (94% [498/527] of respondents). This was measured using a 4-point Likert scale (“definitely would want” to “definitely would not want” the vaccine) in response to the question “Given the information provided, how much would you personally want to receive the HPV vaccine if your OB/GYN provider had it available and recommended it for you?” This response was later dichotomized to definitely/probably would want vs. definitely/probably would not want given the data’s distribution, and because the ultimate decision to receive a vaccine is a yes or no decision. A variety of secondary outcomes among all respondents (i.e. those with and without prior HPV vaccine doses, n = 527) were also assessed. Participants’ perceptions of other women wanting the vaccine were measured using the same 4-point Likert scale, and were assessed for three different hypothetical age categories (27–45 years, 46–65 years, and 66+ years), with and without hypothetical insurance coverage for the vaccine. Participants were also queried about how much they felt they knew about HPV (nothing/a
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little vs. some vs. a lot), whether they had ever discussed the HPV vaccine with their primary care provider, whether primary care providers in general should “routinely talk about the HPV vaccine with their female patients who are over age 26” (4-point Likert from strongly agree to strongly disagree), a variety of reasons why they would or would not want the HPV vaccines for themselves, and whether “they or anyone close to them” had experience with a variety of HPV-related diseases (defined in this study as “personal experience with HPV”). A 7-item series of true/false questions about the virus was used to generate a HPV knowledge ‘score’ for each participant that was later divided into three HPV knowledge categories (low – <58% correct, moderate – 58–83% correct and high – >83% correct) based on the distribution of correct answers. Demographic characteristics assessed included age of the participant (categorized later as 26–34, 35–44, 45–54, and 55+ years), education level (later consolidated to some high school/high school grad vs. some college/college grad vs. advanced degree), household income (later consolidated to <$50 k vs. $50 k–$99,999 k vs. $100 k+), race (later dichotomized to white vs. other), insurance type (later consolidated to public vs. private vs. other), whether they were currently the parent of an adolescent son or daughter, whether or not they had a chronic health condition (defined as any health condition lasting longer than 3 months), and what type of medical provider they saw as their primary care doctor (later categorized as ob-gyn vs. internal/family medicine vs. other). Descriptive statistics were generated for all survey questions. The association between the various outcome measures and predictor variables was assessed using Chi-square, Fisher’s exact or MacNemar’s tests as appropriate. Univariable and multivariable log binomial regression analyses were used to identify independent predictors of participants wanting the HPV vaccine for themselves. The multivariable model included items that were found to be possibly significantly associated (p ≤ 0.1) with this outcome in univariable analyses plus race, age, education, and insurance type, as these have been shown in studies of younger women to be important predictors of HPV vaccination [16,17]. Given the high prevalence of the main outcome, risk ratios (RR) were chosen as the reporting measure rather than OR. Trends of vaccine acceptance across the three age categories for hypothetical older women were assessed using generalized estimating equations to account for repeated measures among participants, and included only those participants who provided an answer for all three hypothetical age categories. All analyses were performed in SAS 9.2 (Cary, NC).
3. Results Less than 1% (5/872) of our survey sample was unable to be reached via email (i.e. email bounce backs). Of those reached, 527 responded to the survey for a response rate of 61%. There were 29 women (5.6% of the total sample) who indicated they had already received the HPV vaccine series, and were therefore excluded from analyses regarding wanting the vaccine for themselves. There was no difference between responders and non-responders in age, pregnancy status or whether they had received the HPV vaccine previously. Table 1 shows the demographic characteristics of 527 respondents. Most women had heard of HPV previously (Table 2). Only 17% of women felt they knew “a lot” about HPV. Consistent with previous studies [11,18–20] a high proportion (76%) of women or “someone close to them” had experienced HPV infection and related sequelae (Table 2). Half of the unvaccinated women in our study indicated they would “probably” or “definitely” get the vaccine if it their provider had it available and recommended it for them. Prevention of cervical cancer was the most common reason endorsed by women
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Table 1 Participant demographics (n = 527).d Characteristic
% (n)
Age 26–34 35–44 45–54 55–77 Education Some high school/high school grad Some college/college grad Advanced degree Race White Other Household income <$50 k $50–99,999 k $100 k+ Prefer not to answer Health Insurance Public Private No insurance/other Parent of an adolescent age 11–17 Has adolescent sona Has adolescent daughtera Has chronic health conditionb Primary care physicianc Ob-gyn Internist/family medicine Other
30% (160) 30% (157) 23% (120) 17% (89) 10% (50) 61% (314) 29% (152) 89% (449) 11% (57) 15% (76) 39% (200) 36% (185) 10% (51) 3% (16) 90% (465) 7% (36) 23% (118) 13% (66) 15% (79) 32% (163) 24% (122) 70% (360) 7% (34)
a Participants could have both sons and daughters who are adolescents, thus summation of these two groups is greater than “parent of adolescent age 11–17.” b Defined as a positive response to the question “Do you have a health condition or health problem that has lasted longer than 3 months?” c Percentages do not add to 100% due to rounding. d Missing values were excluded from the denominator if >10% of the survey sample.
wanting the vaccine (86%, n = 212) followed by “doing what the ob-gyn provider recommends” (42%, n = 103). Only 7% (n = 17) of women endorsed the statement “I think I might be at risk for HPV” as a reason for wanting the vaccine. Among women who did not
want the vaccine, 41% (n = 100) indicated the reason for their decision was because they thought the vaccine would be too expensive, and 39% (n = 95) indicated that they did not think they were at risk for HPV. Eleven percent (n = 26) indicated that they “do not generally get vaccines” as a reason for not wanting the HPV vaccine. In univariable analyses (Table 2) higher self-perceived knowledge about HPV and personal experience with a positive HPV test, genital warts, and cervical cancer were significantly associated with wanting the HPV vaccine for oneself. In multivariable analyses (Table 3) only self-perceived knowledge about HPV remained statistically associated with this outcome when controlling for other variables. Participants were queried whether they believed older women in general would want the vaccine. Separate questions were asked for three age categories of hypothetical women (27–45, 46–65 and 66+), and with or without hypothetical insurance coverage for the vaccine. As shown in Table 4, for each hypothetical age category, a significantly higher proportion of women were believed to want the vaccine if it was covered by insurance. As the age of the hypothetical women increased, there was a statistically significant trend for a decreased proportion of women believed to want the vaccine (Table 4). However, it was notable that even at the highest hypothetical age category being considered (66+ years), a majority of participants (60%) still believed that these oldest women would want the vaccine if covered by insurance. The only consistent predictor of believing other women would want the vaccine was wanting the vaccine for oneself. Overall, 36% of women had discussed the HPV vaccine previously with their primary care provider. In univariable analyses, discussion with the provider was significantly associated with having higher self-reported knowledge about HPV (p < 0.0001) but not the actual knowledge score. It was also associated with being the parent of an adolescent (p = 0.0004), having an ob-gyn as the primary care provider (p = 0.0042), not having a chronic health condition (p = 0.0078), younger age (p < 0.0001), higher education (p = 0.0331), and personal experience with HPV, including known exposure to partner with HPV (p = 0.0014), previous positive HPV test (p = .0005), and having experienced an HPV-related problem previously (p = 0.0036). Prior discussion of HPV vaccine with the
Table 2 Older women’s knowledge and experience with HPV, n = 461.d Characteristic
Sample overall % (n)
Likelihood of getting the HPV vaccine if offered Probably/definitely would get % (n)
Probably not/definitely not would get % (n)
p-Value
Ever heard of HPV before study
94% (461)
94% (231)
94% (230)
Self-report of amount known about HPV Nothing/a little Some A lot
36% (176) 49% (240) 15% (73)
34% (82) 47% (116) 19% (47)
39% (94) 51% (124) 11% (26)
Knowledge scorea Low Moderate High
38% (188) 28% (140) 33% (165)
38% (94) 29% (72) 33% (81)
38% (94) 28% (68) 34% (84)
Abnormal Pap smearb
71% (348)
72% (177)
70% (171)
0.60
Positive HPV testb
26% (127)
30% (73)
22% (54)
0.05
Genital wartsb
21% (103)
26% (63)
16% (40)
0.0116
14% (68)
17% (42)
11% (26)
0.0383
9% (46)
10% (25)
9% (21)
0.55
76% (375)
79% (196)
73% (179)
0.09
0.0284
0.92
b
Cervical cancer
Known exposure to partner with HPVb c
Ever experienced HPV a
>0.99
Categorized using the mean number of correct responses to 7 true/false knowledge questions. b Asked using the stem “Have you or anyone close to you ever had. . .”. c A composite variable defined as positive response to ≥1 HPV related health condition listed above. d Restricted to the subset of women who indicated they had not received prior HPV vaccine doses and had non-missing data. Bold lettering denotes statistically significant results.
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Table 3 Univariable and multivariable associations of definitely or probably wanting the HPV vaccine for oneself if available, n = 461. Variable
Multivariableb
Univariable RR (95% CI)
Age 26–34 35–44 45–54 55–87 Education Some high school/high school grad Some college/college grad Advanced degree Race White Other Household income <$50 k $50–99,999 k $100 k+ Prefer not to answer Health Insurance Public/no insurance/othera Private Parent of an adolescent age 11–17 Has adolescent son Has adolescent daughter Has chronic health condition Primary care physician Ob-gyn Internist/family medicine Other Ever heard of HPV before study Self-report of amount known about HPV Nothing/a little Some A lot Knowledge score Lo Moderate High Ever experienced HPV
p-Value
RR (95% CI)
0.9881
p-Value 0.9765
Ref. 1.03 (0.82, 1.30) 1.00 (0.78, 1.28) 1.00 (0.76, 1.31)
Ref. 1.04 (0.81, 1.32) 1.02 (0.79, 1.32) 1.06 (0.80, 1.40) 0.9206
0.8732
Ref. 0.95 (0.71, 1.27) 0.98 (0.72, 1.34)
Ref. 0.92 (0.69, 1.23) 0.94 (0.68, 1.29) 0.3121
0.1052
Ref. 1.15 (0.89, 1.50)
Ref. 1.27 (0.97, 1.67) –
0.9790
–
Ref. 0.99 (0.75, 1.31) 1.02 (0.77, 1.35) 0.96 (0.66, 1.40) 0.41 Ref. 0.94 (0.71, 1.24) 0.99 (0.81, 1.22) 0.81 (0.60, 1.09) 1.09 (0.87, 1.36) 1.04 (0.87, 1.26)
0.66 Ref. 0.94 (0.71–1.24) 0.97 (0.78, 1.21) –
0.9601 0.1329 0.4828 0.6525 0.4972
Ref. 1.13 (0.90, 1.42) 1.02 (0.67, 1.55) 1.00 (0.67, 1.55)
– –
>0.99 0.0272
–
Ref. 1.04 (0.84, 1.27) 1.40 (1.10, 1.74) Ref. 1.03 (0.83, 1.27) 0.98 (0.79, 1.21) 1.21 (0.96, 1.52)
0.7796 – – – –
– 0.0155
0.92
Ref. 1.03 (0.83, 1.27) 1.43 (1.12, 1.83) –
–
0.0861
1.17 (0.93, 1.48)
0.1675
a
Because of small sample size, “other” insurance was combined with “public” for the analysis. b The model includes only the variables with values listed. Bolded items indicate statistical significance.
provider was not associated with an increased likelihood of wanting the HPV vaccine for oneself. Almost all of the women surveyed (93%) believed that primary care physicians should discuss the HPV vaccine routinely with older women in general. The only factors that were associated with this outcome statistically were personally wanting the HPV vaccine for oneself (p < 0.0001), and having an ob-gyn as the primary care provider (p = 0.0059). 4. Comment In this study of women aged 26–77, half of the participants without prior HPV vaccination indicated they would probably or definitely want the HPV vaccine for themselves in the coming year
if their ob-gyn provider had it available and recommended it for them, even if they had to pay out of pocket for it. Wanting the vaccine for oneself was more prevalent among women who perceived they had a high level of knowledge about HPV, and among women who had prior experience with an HPV-related health condition in themselves or someone close to them. A majority of participants also believed that other older women would want the HPV vaccine if it were covered by insurance. However, the perceived likelihood of other older women wanting the vaccine was significantly less if women had to pay for the vaccine out of pocket. Nearly all women believed that primary care physicians in general should discuss the HPV vaccine routinely with women over age 26 years. In our study there was surprisingly little variation by demographic characteristics in the proportion of women wanting the
Table 4 Participants perceptions of other women wanting the HPV vaccine, by age and insurance, n = 611. Age category of hypothetical older women
27–45 46–65 66+ Trend statistic by agea a
Proportion of participants who perceive other women in general would “definitely” or “probably” want the HPV vaccine (n) If covered by insurance % (n)
If had to pay out of pocket % (n)
97% (496) 84% (435) 60% (303) <0.001
22% (115) 20% (103) 8% (40) <0.001
Analysis limited to those who answered for all three age groups assessed (n = 506 for “covered by insurance”, n = 512 for “pay out of pocket”).
p-Value
<0.001 <0.001 <0.001
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vaccine for themselves, or in the proportion believing that other older women would want the vaccine. The only exceptions to this were age and insurance. The proportion of respondents who believed that other older women would want the vaccine decreased with increasing age of the hypothetical women being considered, and was also markedly lower for all hypothetical age categories if there were no insurance coverage for the vaccine. However, neither age nor insurance status was related to whether a woman wanted the vaccine for herself. The majority of women in our study were insured, with relatively high education and income. Thus one hypothesis to explain this dichotomy in results is that women in our study did not perceive cost as a personal barrier to vaccination, but believed it could be a barrier to other women. To our knowledge there are only a small number of other studies that have examined attitudes about HPV vaccines among older women, and most occurred prior to or shortly after the vaccine’s licensure. In a study by Weiss et al. [21], which was performed in 2007 and included 451 women age 27–45 years, 71% of women surveyed indicated they would be likely or extremely likely to get the vaccine if it were offered in the future. Kahn et al. found that among nurses who were mothers of young women ages 9–18 about 48% would get the vaccine if it were recommended for them [22]. It is unclear whether in these two studies the potential cost of the vaccine was described. If not, this could explain why acceptability of the vaccine was higher in the Weiss study than in ours, where only 50% of women indicated the definitely or probably would want the vaccine if offered in the future. Our results are in keeping, however, with other studies on older women’s attitudes about HPV vaccines by Kahn et al. [22] and Ferris et al. [23,24], in which it was it was reported in 2006 that ∼50% of older women would want to get the HPV vaccine. Reasons for wanting or not wanting the vaccine were similar between both of these studies and our study. Other studies found similarly high acceptability among women 27 to 55, but each also report that cost was a potentially significant barrier to vaccination among this population and was associated with decrease acceptability and likelihood to vaccinate against HPV [25–27]. Current licensure by the FDA means that women over 26 in the U.S. who choose to receive the HPV vaccine would do so off-label, requiring out-of-pocket costs and likely limiting access to women with adequate financial resources. When the vaccine is covered by public and private insurance, vaccination is one of the best ways to reduce certain health disparities. However, this may not feasible for HPV vaccination of women over age 26. In the Ferris study, older women were less likely to endorse wanting to get the vaccine for themselves than younger women. This contrasts with our finding of no association between participant age and wanting the vaccine for oneself. One hypothesis to explain this difference is that our study was performed several years after the Ferris study, during which time public knowledge and awareness about HPV infection and vaccination has risen substantially. Heightened awareness among older women about the burden of HPV in their age group, plus increased public recognition that HPV infection is nearly ubiquitous among the sexually active population, could explain why in our study age appears to no longer be associated with wanting the vaccine. Physician recommendation has been shown to be one of the most consistent predictors of HPV vaccine utilization [28,29]. In our study, participants overwhelmingly believed that the vaccine should be routinely discussed by primary care providers with women over the age of 26. This finding, combined with the suggestion by our results that many women would be willing to pay out of pocket for the vaccine, implies that there may be substantial missed opportunities for HPV prevention among older women. Gynecologists may be in a unique position to enhance the health of women in this regard as they are not only keenly aware of the
potential health effects from HPV infection, but also are the primary care physician for a substantial proportion of mid-adult women, including 24% of the women in our study [30]. Prior research suggests that among medical specialties that serve as primary care providers, vaccines are less likely to be given to patients by gynecologists when compared to family medicine or internal medicine providers [31,32]. However, this is likely to change over time as more vaccines are recommended for pregnant women, allowing ob-gyns to become more experienced at immunization delivery. Moreover, medical organizations have recently identified improving immunization delivery as a priority area for ob-gyns nationally [33]. The question of whether ob-gyn providers should discuss and offer the HPV vaccine to women over the age of 26 is ultimately a balancing act of practice efficiency and maximum vaccine coverage and prevention of the sequelae of HPV infection. While some populations of women, especially those with the means to pay out-of-pocket for the vaccine, may benefit more from a practice of offering the vaccine off-label, practices should also take into account a women’s right to opt for vaccination. Since most women are naïve to at least some of the strains of HPV that vaccines protect against, most women would benefit to some extent from HPV vaccination. Providers and patients should consider discussing the costs and benefits of vaccination with women older than 26 so that each woman can make the right choice about HPV vaccination for themselves. Our study results should be interpreted with certain limitations in mind. First, our study took place within a discrete geographical area, and the study sample was relatively well educated, wealthy, and with little racial or ethnic diversity. Our study’s findings therefore cannot be generalized to other populations, particularly women who are at highest risk for HPV infection and its sequelae such as African Americans and those with lower incomes [34]. In addition, our main outcome measure was hypothetical acceptance of an HPV vaccine for oneself, which may or may not accurately reflect what a woman would do if actually given the opportunity to be vaccinated. In conclusion, in this study of 26–77 year old women, a high proportion (∼50%) would want to be vaccinated against HPV, even if they had to pay for it out of pocket. There was little variability by demographic characteristics among women wanting the vaccine for themselves, suggesting a broad acceptance of this vaccine among older women, and potentially among diverse populations. Though the vaccine is not currently licensed in the U.S. for women over the age of 26, older women still experience a substantial burden of HPV-related diseases and are frequently naïve to at least one HPV strain covered by the vaccine. Our study suggests that if providers were to offer the vaccine to their older patients as part of routine well woman care, many women would choose to get vaccinated. Funding source This work was funded by the Centers for Disease Control and Prevention (5U01-IP000501-03). The opinions expressed in this manuscript do not necessarily represent those of the funding agency. Survey administration through REDCap was supported by NIH/NCRR Colorado CTSI Grant (UL1 TR000154). Conflicts of interest Amanda Dempsey serves on Advisory boards for Merck and Pfizer. These companies played no role in this research study. Dr. Dempsey does not received research support from either company. All other authors have no conflicts of interest to declare.
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