Missed opportunities for HPV immunization among young adult women.

Despite the availability of a safe and cost-effective vaccine against HPV, 23 the uptake of the vaccine in the United States is low. The consequences of maintaining the low HPV immunization rates are not insignificant. In 2017, immunization experts estimated that if the HPV immunization rate could be raised to 80%, an additional 53,000 cases of cervical cancer could be prevented during the lifetime of those younger than 12 years; this is equivalent to 4400 new cases of cervical cancer for every year that the immunization rate does not increase. 24 Missed opportunities for administering the HPV vaccine are a major barrier to achieving high rates of immunization. Several studies in adolescents have identified factors associated with the low uptake of the HPV vaccine, such as a lack of knowledge about it, cost, or reluctance of providers to recommend the vaccine 25 , 26 ; however, less is known about the frequency or characteristics of missed opportunities to administer the vaccine in the young adult population (18–26 years of age). 27 , 28 One qualitative study reported that gaps in knowledge about cervical cancer, HPV, and the HPV vaccine as well as other barriers, such as poor access to transportation and prioritizing other responsibilities over health, were important obstacles to immunization in these women. 29 Our study contributes to the literature by specifically examining patient characteristics and providing detailed descriptive analysis of clinical factors such as the reason for the visit or concomitant care received during a visit. Such information may provide a greater context for missed opportunities for immunization when a woman engages in a clinical visit in a women’s health setting and insight into strategies for addressing these missed opportunities. Our study found that women who self-identify as black were more likely to have had a missed opportunity compared with white women. The racial disparities observed in our study are consistent with previous research reporting that racial minorities, specifically non-Hispanic blacks, are less likely to receive a recommendation to vaccinate from health care providers and are less likely to complete the HPV vaccine series. 30 , 31 Although studies have shown there has been progress in closing the gap in uptake among minorities (particularly among Hispanics and women living below the poverty level), 7 our study suggests there is still disparity among women of the black race. Of note, the cost of the HPV vaccine is covered under most Medicaid plans for women up through 26 years of age. Likewise, most private insurance covers the cost of the vaccine for women up until their 27th birthday. Uninsured women can have the cost of the vaccine covered by the Connecticut Vaccine Program until they turn 19 years of age. 32 Women who are 19 years of age or older and uninsured would need to pay out of pocket for the vaccine, which can range between $150 and $200 per dose. Our study population consisted of women who had access to care and who were predominantly insured through Medicaid. Therefore, the disparity in missed opportunities for HPV immunization among racial and ethnic minorities after controlling for insurance status is especially concerning and warrants further investigation. The disparity may be driven by a multitude of factors including possible provider biases and assumptions, sociocultural beliefs about vaccines and cervical cancer, or perceived quality of patient-provider interactions. Understanding the nature of this disparity can facilitate development of strategies to eliminate missed opportunities for immunization with the HPV vaccine and potentially reduce disparities in cervical dysplasia and cancer. There was no statistically significant association between missed opportunities and preferring either the Spanish or the English language. However, women whose preferred language was one other than Spanish or English were less likely to have a missed opportunity. While our study was not designed to explore this association in greater depth, based on our extensive experience with this diverse patient population, representing 12 different languages, we believe this association could be related to several potential factors. It is possible that many of these women come from cultures where it is improper to question recommendations from an authority figure, and hence, these women are more likely to be agreeable to the vaccine. The combination of this increased willingness to trust in the clinicians with a significant language barrier (eg, women not fully understanding what they are agreeing to) may have contributed to the lower rate of missed opportunities in this population group. Of the missed opportunity visits, 26.5% occurred when another vaccine or injectable medication was administered. These visits are excellent opportunities for providers to encourage patients to receive the HPV immunization because studies have shown that patients are more willing to accept the HPV vaccine when it is viewed as routine or when given with other injections. 33 Although some data suggest that providers are less likely to recommend the HPV vaccine to avoid giving multiple injections in 1 visit, Wallace et al 34 found that providers overestimate concerns of patients about multiple immunizations, and education and reassurance from providers often address these concerns. This suggests that interventions that bundle administration of the HPV vaccine with other vaccines or injectable medications might help avoid missed opportunities in clinics that cater to young adults. In obstetrics and gynecology clinics, many injectable medications (such as medroxyprogesterone acetate) are given during nurse-only visits. In our study, the large number of missed opportunities that occurred when other injectable medications were administered highlights the potential role of nurses in promoting uptake of HPV vaccine and the potential value in developing protocols for the nurse-initiated recommendation of the HPV vaccine. The 2 most common missed opportunity visit types were for contraception and STD screening visits. As Dilley et al 35 recently advocated, these visits could be prime opportunities for women’s health providers to improve the rates of HPV immunization because most of these patients are planning to become or already are sexually active, and a recommendation for HPV vaccine could easily be integrated into a broader discussion of reproductive health and family planning. A common context for missed opportunities among young adult women during our study period were postpartum visits. In contrast to other vaccines such as Tdap (tetanus, diphtheria, and pertussis), influenza, and MMR (measles, mumps, and rubella), the HPV vaccine is not routinely available in the immediate inpatient postpartum period and may not be a priority for patients or providers in follow-up visits in the outpatient setting. 36 One study of more than 48,000 age-eligible, unvaccinated pregnant women found that only 1.8% of the women had received a dose of HPV vaccine during the first postpartum year. 37 Interventions focused on implementing routine HPV immunization during the inpatient postpartum admission and system-generated reminders to complete the immunization series in postpartum follow-up appointments are likely to improve the uptake in this age group. 35 , 38 , 39 Our study has several limitations. This was a single-center study from a clinic that provides care to a predominantly low-income, minority population. Therefore, our findings may not be generalizable to other settings. Future research is needed in different clinical settings to validate our findings and inform the generalizability of our results. Our data also relied on electronic medical records from a single health care system; immunizations administered by providers not affiliated with our system may not have been completely captured. This may result in a potential overestimation of missed opportunities. However, in our study population, this is unlikely to have been a major issue. In a different study from our institution, a sample of adult women who sought care at our clinic were interviewed to assess all prior sources of care since 2006, when the HPV vaccine was introduced. We found that an accurate HPV vaccine history could be ascertained in 82% of these women by reviewing electronic medical records because the majority of these adult women received care either exclusively at our clinic or at one of the other sites within the Yale–New Haven Hospital System (unpublished data). In the self-report designations of race and ethnicity, the majority of women who designated themselves as being of Hispanic ethnicity did not provide a particular race, which is why we used a combined race/ethnicity variable. Lastly, the data collection focused on detailed information about the missed opportunity visits. Similar information was not obtained about opportunities at which patients were immunized. Because only 3.1% of women appropriately received a dose of the HPV vaccine during the study period without any missed opportunity, the validity of comparisons of those visits would be impaired by poor statistical power. This study, conducted in a diverse urban population, found that a majority of underimmunized vaccine-eligible young-adult women (18–26 years of age) had at least 1 missed opportunity in their interaction with an obstetrics and gynecology clinic over a 1 year study period, most of which were related to postpartum visits or to visits for either contraception or STD screening. Interventions that aim to eliminate these missed opportunities are likely to improve the uptake of the HPV vaccine in this population of young adult women.

During the 1 year study period, a total of 1410 women, 18–26 years of age, had a total of 6988 visits, with a mean of 4.9 visits per person. Of these women, 169 (11.9%) had received 3 doses of the HPV vaccine prior to the study period and were excluded from the analyses ( Figure 1 ). The final group included 1241 age-eligible women who were underimmunized (had received <3 doses of the HPV vaccine) and had at least 1 visit during the study period. Of the underimmunized women, 833 (67.1%) had at least 1 missed opportunity for immunization, 362 (29.2%) had noneligible pregnancy visits, 39 (3.1%) received a dose during the study period and did not have any further eligible visits, and 7 (0.6%) were offered the vaccine and declined it. Of the 833 underimmunized women, there was a mean of 1.3 (range 0–9) missed opportunities per person. Women eligible to receive their first dose were equally likely to have a missed opportunity compared with those who were eligible to receive their second or third dose (odds ratio, 0.72 [95% confidence interval (CI), 0.48–1.08]; P = .11). Characteristics of the underimmunized women and women with at least 1 missed opportunity are shown in Table 1 . The types of visits that were associated with missed opportunities are shown in Figure 2 . The most common types were visits for contraception (33%; for medroxyprogesterone acetate [58%] and other types of contraception [42%]), visits for sexually transmitted disease (STD) screening (21%), and postpartum visits (17%). Of the patients with a missed opportunity, 221 (26.5%) had at least 1 vaccine-eligible visit at which an injectable medication (medroxyprogesterone acetate) or a different vaccine was administered. Results from simple and multivariable logistic regression are detailed in Table 2 . The independent variables included in the final model were race, preferred language, and insurance. Women who identified their race as black had 61% higher adjusted odds of having a missed opportunity compared with white women (adjusted odds ratio [aOR], 1.61 [95% CI, 1.08–2.41]; P =.02). Women who identified their preferred language as other than English or Spanish were less likely to have a missed opportunity compared with preferred English speakers (aOR, 0.25 [95% CI, 0.07–0.87]; P =.03). Associations between missed opportunities and age, Hispanic ethnicity, Spanish language, or parity were not statistically significant.

In this cross-sectional study, electronic medical records were reviewed for all women 18–26 years of age who were underimmunized (had received 0, 1, or 2 doses of the HPV vaccine), who were vaccine eligible and who were seen at the Yale New Haven Hospital Women’s Center, a hospital-based obstetrics and gynecology clinic that serves primarily low-income patients of racial and ethnic minority backgrounds, from February 1, 2013, to January 31, 2014. Using a standardized form, data were collected regarding the number of visits, sociodemographic variables (age, race, ethnicity, preferred language, insurance), pregnancy status, and receipt of HPV vaccine. Additional data were collected for the subset of women considered to have missed opportunities (see the following text), which included reasons for visits as documented in the clinic note as well as documentation of administration of other immunizations and injectable medications. HPV immunization status was determined by evaluating the immunization history section of the electronic medical record in which the dates of vaccine administration are documented and reviewing all Women’s Center clinic notes and scanned records from the study period for the mention of receipt or offer of the HPV vaccine by a provider. The Institutional Review Board at Yale University approved this project. A vaccine-eligible visit was defined as a visit at which the patient was between 18 and 26 years of age, was not pregnant, and was underimmunized or had never been immunized. A missed opportunity was defined as a vaccine-eligible visit at which the patient was due for either the first, second, or third dose of the HPV vaccine but it was not administered. The recommendations from the CDC’s Advisory Committee on Immunization Practices are that any available HPV vaccine product (bivalent, quadrivalent, or nonavalent) be used to continue or complete the series for protection against HPV 16 and 18. 6 Accordingly, we considered the use of any HPV vaccine as a capitalized opportunity. If the patient had received a dose of the vaccine before the visit, the patient was not defined as eligible for another dose until at least 8 weeks after a first dose or 16 weeks after the second dose (and 24 weeks between the first and third dose). Insurance was classified as public, private, uninsured, and other. Public insurance included Medicaid, Medicare, Indian Health Service, and military insurance. Self-reported race and ethnicity were classified as non-Hispanic white, non-Hispanic black (subsequently referred to as white and black, respectively), His-panic, and non-Hispanic other. Logistic regression models were estimated to identify patient characteristics associated with at least 1 missed opportunity for HPV immunization during the 1 year study period. All patient characteristics were first evaluated individually for association with missed opportunities using simple regression models (ie, including 1 patient characteristic at a time). For the multivariable logistic regression model, backward stepwise selection was used to select the final group of variables, in which variables with the highest p-values were removed in sequence until all variables in the final model had a value of P ≤.1. A value of P <.05 was considered to be statistically significant. This is a descriptive and exploratory study utilizing a convenience sample consisting of the number of women who attended the clinic during a 12 month period. Data were analyzed using Stata statistical software 12.0 (StataCorp, College Station, TX).