Abstract
Background: It has been reported that Pap smear use is higher among U.S. women who received the human papillomavirus (HPV) vaccine than unvaccinated women. This study assessed the role of provider and patient in the difference of Pap smear use by vaccination status.
Methods: We conducted a cross-sectional study of 5416 young women (21–30 years of age) with detailed information on Pap smear use and HPV vaccination status from the National Health Interview Survey (NHIS) 2013–2015. Vaccinated women received at least one dose of HPV vaccine. Main outcomes included Pap smear in the past year, provider's recommendation for Pap smear, and patient-initiated Pap smear.
Results: The prevalence of Pap smear in the past year was much higher among vaccinated women than unvaccinated women (67.5% vs. 52.8%, p < 0.001). Compared with unvaccinated women, vaccinated women were more likely to receive a provider's recommendation for Pap testing (60.8% vs. 50.8%, p < 0.001), to obtain Pap testing after receiving a provider's recommendation (75.1% vs. 67.9%, p = 0.004), and to initiate Pap testing themselves (57.7% vs. 38.2%, p < 0.001). However, among women who visited an obstetrician/gynecologist (OB/GYN) in the past year, the positive association between HPV vaccination and Pap smear recommendation and uptake vanished.
Conclusions: Unvaccinated women who have not visited an OB/GYN in the past year are less likely to receive a recommendation for Pap testing from their providers or to initiate Pap testing themselves without a provider's recommendation. They should be encouraged to visit an OB/GYN provider for cervical cancer screening.
Keywords: : human papillomavirus vaccine, cervical cancer, papanicolaou test, cancer screening, health communication
Introduction
Cervical cancer is caused by oncogenic types of human papillomavirus (HPV).1,2 In women, to prevent HPV infection, vaccination is recommended for girls 9–12 years of age, with catchup vaccination up to 26 years in the United States. In other countries, the recommended age for HPV vaccine varies slightly. For example, Australia recommends vaccination among girls 12–13 years of age with a time-limited catch-up program (women aged 14–26 years), and is recommended for girls 11–14 years of age in Canada. The HPV vaccine can reduce vaccine-type HPV infections and abnormal Papanicolaou (Pap) test results,3–8 but shows little protection against nonvaccine oncogenic types in postmarket surveillance.9,10 Moreover, it has no efficacy against prior infections.7,11 As such, cervical cancer screening is still essential for cancer prevention.
National guidelines in the United States currently recommend that women undergo Pap testing at 3-year intervals starting at 21 years of age and HPV DNA testing starting at 30 years of age, regardless of HPV vaccination status.12–14 HPV vaccination and Pap smears are preventive care recommended by the U.S. Preventive Services Task Force (USPSTF), and are freely available to women with health insurance coverage (private insurance, or public insurance, such as Medicaid) as required by the Affordable Care Act (ACA).12
However, before ACA was issued in 2010, cervical care coverage by health insurance program varied. Assistance programs, such as the Vaccines for Children (VFC) program, and the National Breast and Cervical Cancer Early Detection Program (NBCCEDP), provide free HPV vaccines and cervical screening to low-income and uninsured women to reduce disparities in cervical cancer incidence.15–17
It has been reported that Pap smear use is higher among young women vaccinated against HPV in the United States.18 A positive association between HPV vaccination and Pap smear uptake has been observed across race/ethnicity and socioeconomic status.19
We have studied the role of provider-patient communications in cancer screening service utilization, and found that providers' recommendations for cancer screening tests are essential for both the proper use of screening services in eligible women20 and overutilization of cervical cancer screening among certain female populations. These include women who are recommended not to receive Pap testing, such as those over 65 years with adequate prior screening and no history of precancerous cervical lesions and those who have had a total hysterectomy for noncancerous conditions.21,22 On the other hand, about 20%–25% of screening services are requested by the patients themselves among women.21,22
In this study, we assessed differences in provider's recommendation for Pap testing and patient-initiated Pap testing between vaccinated and unvaccinated women, using data from the National Health Interview Survey (NHIS) 2013–2015.
Methods
NHIS collected health information through an annual, in-person household survey from a representative cross-sectional noninstitutionalized sample to assess the health status and behaviors of U.S. adults. NHIS used a complex, stratified, multistage sample design to provide nationally representative data. Verbal consent for survey participation was provided by each subject.
We included data from NHIS 2013 to 2015, which had detailed information on HPV vaccination status, Pap smear use, personal history of cervical cancer, and history of hysterectomy. We combined data from those 2 years to generate reliable estimates. After excluding women with a history of hysterectomy (n = 39), history of cervical cancer (n = 44), no valid information on Pap smear use (n = 276), and Pap testing performed for a health problem (n = 216), we had 5416 young women (21–30 years old) remaining in the analyses. This study was exempt from full board review by the Institutional Review Board at University of Texas Medical Branch.
NHIS obtained information about the most recent Pap smear, as well as whether and when the HPV vaccine was received, and doses of vaccine administrated. The time of the most recent Pap smear was recoded using the NHIS 2000 method by combining information contained in month/year, days/weeks/months/years ago, the original time interval grouping, and the interview date. HPV vaccination status was derived from the following questions: “Have you ever received an HPV shot or vaccine?,” “How many HPV shots did you receive?,” and “How old were you when you received your first HPV shot?”. Vaccinated women received at least one dose of HPV vaccine.
Women were also asked whether they had received recommendations for Pap smears from their providers “Was your most recent Pap test recommended by a doctor or other health professional?” or “In the past 12 months, has a doctor or other health professional recommended that you have a PAP test?” If they had not received a provider's recommendation for Pap testing, but obtained a Pap smear anyway, they were determined as having initiated Pap testing themselves.
Age was classified into two groups: 21–25 and 26–30 years of age. NHIS data are from a nationally representative sample. Estimates of HPV vaccination rates among women in these two age groups were comparable between NHIS and The National Health and Nutrition Examination Survey (NHANES), another national survey in the United States.23
Race was self-reported as non-Hispanic white, non-Hispanic black, Hispanic, and other. Immigration status included born in the United States, and not born in the United States. Regions of residence included Northeast, Midwest, South, and West. We also included education level in the analyses: <high school, high school, and >high school.
NHIS collected information on health insurance coverage (public, private, and none) and usual place of healthcare. Those who listed the emergency room as their usual place of healthcare were combined with those who reported no access to a usual source of care. We also included whether participants had visited an obstetrician/gynecologist (OB/GYN), a nurse practitioner/physician assistant/midwife, or other healthcare provider (e.g., general doctor, therapist, and medical specialist) in the past 12 months, as visiting an OB/GYN was associated with Pap smear use.20–22
We compared prevalence of Pap testing in the past 3 years or in the past year between vaccinated women and unvaccinated women from NHIS 2013 to 2015 and assessed the role of providers and patients in the initiation of Pap testing. We used Pap smear utilization in the past year as an outcome of interest, because this study aimed to examine the effect of providers' recommendations for Pap smears in the past year on uptake of Pap smear by vaccination status. We also assessed how visiting an OB/GYN in the past year affected the relationship between HPV vaccination and Pap smear use.
Multivariate logistic regression models were used to assess differences in screening use and recommendation received by vaccination status. Controlled variables included age, race/ethnicity, region of residence, insurance type, and education level. Adjusted prevalence ratios were obtained from average marginal predictions in the fitted logistic regression model.24,25
Sample weights of final annual person weights were incorporated into all analyses through a “weight” statement in SAS survey analysis procedures following NHIS analyses guidelines,26 to account for differential probabilities of selection and the complex sample design, and nonresponse and noncoverage. Sensitivity analysis was performed by excluding women who received the first dose of HPV vaccine after 26 years of age. Statistical analyses were conducted using SAS software version 9.4 (SAS Institute, Cary, NC) and SAS-callable SUDAAN software version 11 (Research Triangle Institute, Research Triangle Park, NC). A two-sided p-value <0.05 was considered statistically significant.
Results
Among 5416 young women from NHIS 2013 to 2015, the proportion of women who received a Pap smear in the past 3 year was much higher among vaccinated than unvaccinated women (88.4% vs. 75.6%, adjusted prevalence ratio 1.17, 95% confidence interval [CI] 1.13–1.21, Table 1). The proportion of women who received a Pap smear in the past year was also much higher among vaccinated than unvaccinated women (67.5% vs. 52.8%, p < 0.001, Table 2). The higher utilization of Pap testing among vaccinated women was observed across all subgroups. Compared with unvaccinated women, vaccinated women were more likely to have a college education, to have private health insurance coverage, to have a usual place of care, and to have visited an OB/GYN in the past year.
Table 1.
Screening Pap Smear in the Past 3 Years Among Young Women According to Human Papillomavirus Vaccination Status, National Health Interview Survey 2013–2015 (N = 5416)
| Pap smear in the past 3 years | |||||
|---|---|---|---|---|---|
| n (%)a | % (95% CI) | ||||
| Characteristics | Vaccinated | Unvaccinated | Vaccinated | Unvaccinated | Adjusted PRb(95% CI) |
| Total | 1618 (29.9) | 3798 (70.1) | 88.4 (86.3–90.5) | 75.6 (73.7–77.5) | 1.17 (1.13–1.21) |
| Age | |||||
| 21–25 | 941 (18.9) | 1557 (32.4) | 84.1 (80.9–87.4) | 66.5 (63.3–69.7) | 1.23 (1.15–1.32) |
| 26–30 | 677 (10.9) | 2241 (37.7) | 95.7 (94.0–97.4) | 83.4 (81.4–85.5) | 1.13 (1.1–1.17) |
| Race/ethnicity | |||||
| NH-white | 946 (19.0) | 1792 (38.6) | 90.1 (87.5–92.7) | 79.3 (76.5–82.1) | 1.14 (1.09–1.2) |
| NH-black | 221 (3.6) | 630 (9.9) | 89.9 (85.2–94.5) | 81.6 (77.6–85.7) | 1.1 (1.03–1.18) |
| Hispanic | 285 (4.9) | 954 (14.9) | 83.0 (76.6–89.5) | 69.5 (65.9–73.0) | 1.19 (1.09–1.31) |
| Other | 166 (2.4) | 422 (6.7) | 83.3 (75.2–91.3) | 59.2 (52.7–65.6) | 1.46 (1.27–1.67) |
| Immigration status | |||||
| Born in the United States | 1469 (27.3) | 2971 (56.4) | 88.8 (86.7–90.9) | 78.6 (76.4–80.7) | 1.14 (1.1–1.18) |
| Not born in the United States | 149 (2.6) | 827 (13.7) | 83.6 (75.4–91.8) | 63.4 (59.4–67.4) | 1.32 (1.19–1.48) |
| Region of residence | |||||
| Northeast | 292 (5.9) | 464 (10.2) | 89.6 (85.0–94.2) | 77.1 (71.9–82.2) | 1.15 (1.06–1.25) |
| Midwest | 333 (6.5) | 774 (15.9) | 88.9 (83.9–94.0) | 77.0 (72.3–81.7) | 1.18 (1.08–1.28) |
| South | 552 (10.0) | 1501 (27.9) | 88.3 (85.0–91.6) | 76.9 (74.2–79.6) | 1.14 (1.08–1.21) |
| West | 441 (7.5) | 1059 (16.2) | 86.9 (82.7–91.2) | 71.1 (67.4–74.9) | 1.23 (1.15–1.32) |
| Education level | |||||
| <High school | 69 (1.4) | 485 (7.4) | 86.1 (74.8–97.4) | 72.1 (66.2–77.9) | 1.16 (0.98–1.36) |
| High school | 215 (4.0) | 880 (16.7) | 91.7 (87.2–96.1) | 73.3 (69.4–77.1) | 1.26 (1.17–1.36) |
| >High school | 1334 (24.5) | 2423 (45.8) | 87.9 (85.6–90.3) | 77.0 (74.6–79.4) | 1.16 (1.12–1.21) |
| Missing | 10 | ||||
| Health insurance coverage | |||||
| None | 197 (3.1) | 882 (15.6) | 82.5 (75.5–89.5) | 61.1 (57.1–65.1) | 1.36 (1.24–1.5) |
| Private | 1087 (20.7) | 1949 (38.8) | 88.5 (85.8–91.1) | 78.8 (76.1–81.5) | 1.15 (1.1–1.21) |
| Public | 323 (5.9) | 951 (15.3) | 91.3 (86.6–96.0) | 83.1 (80.0–86.2) | 1.11 (1.04–1.18) |
| Missing | 11 | 16 | |||
| Having a usual source of care | |||||
| No | 315 (5.5) | 946 (17.0) | 80.9 (75.4–86.4) | 64.8 (61.0–68.6) | 1.22 (1.12–1.34) |
| Yes | 1303 (24.4) | 2851 (53.1) | 90.0 (87.7–92.4) | 79.1 (76.9–81.2) | 1.16 (1.11–1.2) |
| Missing | 1 | ||||
| Visiting an OB/GYN in the past year | |||||
| No | 624 (11.2) | 1968 (35.7) | 74.6 (70.1–79.1) | 57.3 (54.4–60.3) | 1.32 (1.21–1.43) |
| Yes | 992 (18.6) | 1829 (34.4) | 96.6 (95.1–98.1) | 94.6 (93.0–96.1) | 1.03 (1–1.05) |
| Missing | 2 | 1 | |||
Bold indicates statistical significance (p < 0.05).
Sample weights were used to calculated weighted percentage.
Adjusted prevalence ratio (vaccinated women vs. unvaccinated women) was adjusted for age, race/ethnicity, region of residence, insurance type, and education level.
CI, confidence interval; NH-black, non-Hispanic black; NHIS, National Health Interview Survey; NH-white, non-Hispanic white; OB/GYN, obstetrician/gynecologist; PAP, Papanicolaou; PR, prevalence ratio.
Table 2.
Screening Pap Smear in the Past 12 Months Among Young Women According to Human Papillomavirus Vaccination Status, National Health Interview Survey 2013–2015 (N = 5416)
| Pap smear in the past year | |||
|---|---|---|---|
| % (95% CI) | |||
| Characteristics | Vaccinated (n = 1618) | Unvaccinated (n = 3798) | Adjusted PRa(95% CI) |
| Total | 67.5 (64.2–70.8) | 52.8 (50.7–54.9) | 1.27 (1.19–1.34) |
| Age | |||
| 21–25 | 63.6 (59.1–68.1) | 45.4 (42.3–48.6) | 1.34 (1.21–1.48) |
| 26–30 | 74.3 (69.7–79.0) | 59.2 (56.3–62.0) | 1.21 (1.12–1.31) |
| Race/ethnicity | |||
| NH-white | 67.4 (63.1–71.7) | 54.1 (51.1–57.2) | 1.23 (1.13–1.34) |
| NH-black | 75.4 (68.5–82.2) | 64.7 (59.9–69.4) | 1.16 (1.03–1.29) |
| Hispanic | 64.0 (56.8–71.3) | 48.6 (45.0–52.2) | 1.29 (1.13–1.48) |
| Other | 63.7 (52.9–74.5) | 37.4 (30.9–43.9) | 1.74 (1.36–2.23) |
| Immigration status | |||
| Born in the United States | 68.6 (65.2–71.9) | 55.2 (52.8–57.7) | 1.24 (1.16–1.32) |
| Not born in the United States | 56.0 (45.1–66.9) | 43.0 (39.2–46.8) | 1.29 (1.05–1.6) |
| Region of residence | |||
| Northeast | 78.1 (71.7–84.4) | 58.7 (52.9–64.6) | 1.34 (1.18–1.51) |
| Midwest | 68.0 (61.7–74.3) | 53.6 (48.5–58.7) | 1.31 (1.18–1.45) |
| South | 69.6 (63.9–75.2) | 54.9 (51.9–57.9) | 1.24 (1.12–1.37) |
| West | 56.0 (48.4–63.6) | 44.8 (40.8–48.9) | 1.24 (1.05–1.46) |
| Education level | |||
| <High school | 62.3 (47.1–77.5) | 45.4 (39.0–51.8) | 1.32 (1–1.75) |
| High school | 68.6 (59.2–78.0) | 49.6 (45.6–53.6) | 1.35 (1.15–1.57) |
| >High school | 67.6 (64.2–71.0) | 55.3 (52.6–57.9) | 1.25 (1.17–1.34) |
| Health insurance coverage | |||
| None | 49.9 (40.7–59.1) | 37.9 (34.0–41.8) | 1.32 (1.09–1.62) |
| Private | 69.0 (65.0–73.0) | 56.4 (53.4–59.4) | 1.26 (1.17–1.37) |
| Public | 71.7 (64.3–79.0) | 59.3 (55.3–63.3) | 1.22 (1.08–1.38) |
| Having a usual source of care | |||
| No | 52.2 (44.6–59.8) | 38.8 (34.5–43.2) | 1.27 (1.06–1.54) |
| Yes | 71.0 (67.3–74.6) | 57.3 (54.9–59.7) | 1.26 (1.18–1.34) |
| Visiting a care provider in the past yearb | |||
| An OB/GYN | 84.5 (81.4–87.6) | 81.1 (78.7–83.4) | 1.04 (0.99–1.09) |
| A NP/PA/midwife | 47.9 (37.9–58.0) | 32.8 (25.9–39.7) | 1.56 (1.19–2.05) |
| Other care provider | 39.4 (33.0–45.9) | 28.4 (25.5–31.3) | 1.48 (1.22–1.79) |
Bold indicates statistical significance (p < 0.05).
Adjusted prevalence ratio (vaccinated women vs. unvaccinated women) was adjusted for age, race/ethnicity, region of residence, insurance type, and education level.
Young adult women who did not visit any care provider in the past year (n = 256, including 31 vaccinated women and 225 unvaccinated women) were excluded from analysis.
NP/PA, nurse practitioner/physician assistant.
Compared with unvaccinated women, those who had been vaccinated against HPV were more likely to have received a provider's recommendation for a Pap smear (60.8% vs. 50.8%, adjusted prevalence ratio 1.17, 95% CI 1.09–1.25, p < 0.001, Table 3), and had a higher likelihood of obtaining a Pap smear in the past year after receiving a provider's recommendation (75.1% vs. 67.9%, p = 0.004, Table 4). Among those who did not receive a provider's recommendation, vaccinated women still had a higher likelihood of receiving a Pap smear (57.7% vs. 38.2%, p < 0.001).
Table 3.
Provider's Recommendation for Pap Smear Among Young Women According to Human Papillomavirus Vaccination Status, National Health Interview Survey 2013–2015 (N = 5355)
| Provider's recommendation % (95% CI) | |||
|---|---|---|---|
| Characteristics | Vaccinated (n = 1603) | Unvaccinated (n = 3752) | Adjusted PRa(95% CI) |
| Total | 60.8 (57.4–64.3) | 50.8 (48.7–52.9) | 1.17 (1.09–1.25) |
| Age | |||
| 21–25 | 58.4 (54.0–62.9) | 47.2 (43.7–50.7) | 1.18 (1.06–1.3) |
| 26–30 | 64.9 (59.7–70.1) | 53.9 (51.3–56.4) | 1.17 (1.06–1.28) |
| Race/ethnicity | |||
| NH-white | 63.8 (59.6–68.1) | 52.3 (48.9–55.6) | 1.2 (1.1–1.31) |
| NH-black | 47.5 (38.6–56.3) | 54.9 (50.2–59.7) | 0.85 (0.69–1.05) |
| Hispanic | 58.4 (50.6–66.2) | 46.4 (42.7–50.0) | 1.22 (1.05–1.41) |
| Other | 62.3 (51.3–73.2) | 45.9 (39.7–52.2) | 1.36 (1.09–1.69) |
| Immigration status | |||
| Born in the United States | 61.5 (57.9–65.1) | 52.1 (49.7–54.6) | 1.17 (1.09–1.25) |
| Not born in the United States | 53.5 (42.9–64.1) | 45.2 (40.7–49.7) | 1.15 (0.93–1.42) |
| Region of residence | |||
| Northeast | 70.6 (63.6–77.6) | 58.1 (52.7–63.5) | 1.16 (1.01–1.33) |
| Midwest | 63.4 (56.5–70.3) | 51.8 (46.6–57.1) | 1.23 (1.09–1.38) |
| South | 55.8 (50.5–61.0) | 49.9 (46.4–53.4) | 1.1 (0.98–1.25) |
| West | 57.5 (49.5–65.6) | 46.7 (43.3–50.1) | 1.21 (1.05–1.39) |
| Education level | |||
| <High school | 67.7 (53.0–82.3) | 48.0 (42.3–53.7) | 1.28 (0.97–1.69) |
| High school | 53.5 (43.8–63.2) | 49.2 (45.1–53.3) | 1.08 (0.89–1.31) |
| >High school | 61.6 (57.8–65.4) | 51.8 (49.0–54.6) | 1.18 (1.09–1.28) |
| Health insurance coverage | |||
| None | 46.3 (37.6–55.1) | 37.9 (34.0–41.8) | 1.25 (1.02–1.54) |
| Private | 62.7 (58.7–66.6) | 51.8 (48.7–54.9) | 1.23 (1.13–1.33) |
| Public | 62.0 (54.3–69.6) | 61.7 (58.0–65.4) | 1 (0.88–1.14) |
| Having a usual source of care | |||
| No | 42.3 (35.5–49.1) | 37.2 (33.4–41.0) | 1.08 (0.89–1.31) |
| Yes | 65.0 (61.2–68.9) | 55.2 (52.7–57.7) | 1.18 (1.09–1.26) |
| Visiting a care provider in the past year | |||
| An OB/GYN | 66.0 (61.5–70.6) | 64.4 (61.3–67.5) | 1.02 (0.93–1.11) |
| A NP/PA/midwife | 52.7 (42.1–63.4) | 49.1 (41.4–56.8) | 1.07 (0.83–1.38) |
| Other care provider | 56.4 (49.9–62.9) | 41.3 (37.7–44.9) | 1.37 (1.19–1.58) |
Bold indicates statistical significance (p < 0.05).
Young adult women with missing data on the status of provider's recommendation for Pap testing (n = 61) were excluded from analysis.
Adjusted prevalence ratio (vaccinated women vs. unvaccinated women) was adjusted for age, race/ethnicity, region of residence, insurance type, and education level.
Table 4.
Pap Smear in the Past Year Among Young Women Who Had Received and Had Not Received Provider's Recommendation for Pap Smear, National Health Interview Survey 2013–2015 (N = 5355)
| Among recommendeda | Among unrecommendedc | |||||
|---|---|---|---|---|---|---|
| % (95% CI) | % (95% CI) | |||||
| Characteristics | Vaccinated (n = 968) | Unvaccinated (n = 1903) | Adjusted PRb(95% CI) | Vaccinated (n = 635) | Unvaccinated (n = 1849) | Adjusted PRb(95% CI) |
| Total | 75.1 (71.4–78.9) | 67.9 (65.4–70.5) | 1.1 (1.03–1.17) | 57.7 (52.0–63.4) | 38.2 (35.2–41.1) | 1.51 (1.33–1.72) |
| Age | ||||||
| 21–25 | 73.5 (68.3–78.8) | 64.9 (60.3–69.4) | 1.12 (1.01–1.23) | 52.4 (45.2–59.6) | 29.1 (25.2–32.9) | 1.7 (1.38–2.1) |
| 26–30 | 77.6 (72.3–82.9) | 70.2 (66.9–73.5) | 1.09 (1–1.19) | 68.3 (60.6–76.1) | 47.1 (43.0–51.1) | 1.35 (1.16–1.57) |
| Race/ethnicity | ||||||
| NH-white | 73.1 (68.2–78.1) | 67.4 (63.7–71.1) | 1.07 (0.98–1.17) | 59.8 (52.2–67.5) | 40.3 (35.9–44.7) | 1.48 (1.25–1.74) |
| NH-black | 80.4 (71.1–89.6) | 79.3 (73.6–84.9) | 1.01 (0.89–1.14) | 70.8 (61.0–80.7) | 47.4 (40.5–54.2) | 1.48 (1.21–1.82) |
| Hispanic | 80.2 (72.8–87.6) | 66.1 (60.4–71.8) | 1.22 (1.07–1.39) | 43.6 (32.1–55.0) | 34.2 (30.0–38.4) | 1.26 (0.94–1.69) |
| Other | 75.7 (65.3–86.0) | 55.1 (45.0–65.2) | 1.35 (1.08–1.69) | 45.7 (29.1–62.3) | 24.5 (17.1–31.8) | 2.11 (1.32–3.38) |
| Immigration status | ||||||
| Born in the United States | 75.3 (71.4–79.2) | 69.0 (66.2–71.8) | 1.09 (1.02–1.16) | 60.0 (54.2–65.9) | 41.1 (37.7–44.6) | 1.47 (1.29–1.68) |
| Not born in the United States | 73.3 (61.1–85.5) | 63.0 (56.5–69.5) | 1.18 (0.97–1.42) | 37.1 (20.6–53.7) | 27.5 (22.7–32.4) | 1.33 (0.84–2.11) |
| Region of residence | ||||||
| Northeast | 83.8 (77.7–90.0) | 70.7 (64.0–77.4) | 1.2 (1.06–1.36) | 64.8 (53.4–76.2) | 41.6 (33.8–49.3) | 1.56 (1.2–2.04) |
| Midwest | 76.0 (69.3–82.6) | 69.8 (64.3–75.3) | 1.11 (1–1.23) | 57.4 (45.6–69.3) | 37.0 (30.5–43.6) | 1.68 (1.27–2.23) |
| South | 75.8 (68.1–83.4) | 70.2 (66.8–73.6) | 1.08 (0.97–1.21) | 63.8 (54.9–72.6) | 40.5 (35.6–45.4) | 1.51 (1.24–1.83) |
| West | 65.0 (55.9–74.0) | 59.6 (53.2–66.0) | 1.07 (0.89–1.28) | 45.5 (33.8–57.2) | 33.7 (28.7–38.7) | 1.34 (1.02–1.77) |
| Education level | ||||||
| <High school | 75.0 (58.6–91.3) | 59.9 (50.7–69.2) | 1.28 (0.97–1.69) | 35.8 (13.0–58.6) | 33.4 (25.3–41.4) | 0.98 (0.48–1.99) |
| High school | 83.4 (73.7–93.1) | 67.0 (61.7–72.2) | 1.22 (1.04–1.42) | 53.1 (38.7–67.6) | 33.5 (28.0–38.9) | 1.59 (1.18–2.15) |
| >High school | 74.0 (69.9–78.0) | 69.6 (66.3–72.8) | 1.08 (1–1.16) | 59.7 (53.6–65.7) | 40.8 (37.1–44.6) | 1.52 (1.32–1.75) |
| Health insurance coverage | ||||||
| None | 64.5 (52.2–76.8) | 59.0 (52.6–65.4) | 1.09 (0.89–1.34) | 37.4 (25.2–49.7) | 25.6 (21.3–29.9) | 1.47 (1.02–2.11) |
| Private | 75.6 (71.1–80.2) | 70.5 (66.9–74.1) | 1.09 (1–1.18) | 60.4 (53.3–67.4) | 42.5 (38.2–46.7) | 1.51 (1.29–1.76) |
| Public | 78.1 (70.1–86.0) | 68.7 (63.6–73.7) | 1.14 (0.99–1.3) | 62.2 (50.0–74.5) | 45.5 (40.0–51.1) | 1.47 (1.15–1.88) |
| Having a usual source of care | ||||||
| No | 64.3 (53.9–74.7) | 58.0 (51.3–64.7) | 1.05 (0.86–1.27) | 44.3 (33.7–54.9) | 28.0 (23.4–32.5) | 1.45 (1.06–1.99) |
| Yes | 76.7 (72.6–80.8) | 70.1 (67.3–72.8) | 1.1 (1.03–1.18) | 62.7 (56.3–69.1) | 42.8 (39.2–46.4) | 1.53 (1.33–1.76) |
| Visiting a care provider in the past year | ||||||
| An OB/GYN | 87.8 (84.6–91.0) | 85.2 (83.0–87.5) | 1.03 (0.98–1.07) | 78.2 (71.7–84.6) | 74.2 (69.5–78.9) | 1.07 (0.96–1.19) |
| A NP/PA/midwife | 52.2 (38.5–65.8) | 43.4 (33.1–53.7) | 1.15 (0.83–1.6) | 45.2 (29.5–60.9) | 24.9 (16.0–33.7) | 2.07 (1.35–3.16) |
| Other care provider | 45.8 (36.6–55.0) | 38.0 (33.2–42.9) | 1.28 (1.14–1.60) | 34.8 (24.7–44.9) | 22.2 (18.3–26.0) | 1.67 (1.20–2.33) |
Bold indicates statistical significance (p < 0.05).
Young adult women with missing data on the status of provider's recommendation for Pap testing (n = 61) were excluded from analysis.
Proportion of women who had a Pap smear in the past 12 months among those who received provider's recommendations for Pap testing.
Adjusted prevalence ratio (vaccinated women vs. unvaccinated women) was adjusted for age, race/ethnicity, region of residence, insurance type, and education level.
Proportion of women who had a Pap smear in the past 12 months among those who had not received provider's recommendations for Pap testing.
Among vaccinated women, 66.9% of Pap tests were received under providers' recommendations, and 33.1% of Pap tests were initiated by women themselves. Among unvaccinated women, 64.7% of women who received Pap tests had recommendations for them by their providers and 35.3% initiated by patients who did not have a health provider recommendation for a Pap smear.
There was no relationship between doses of HPV vaccine received and Pap smear in the past 3 years or in the past year (Fig. 1). Proportions of young vaccinated women who received a Pap smear in the past 3 years or in the past year were similar across doses of HPV vaccine received. Young women who received one, two, or three doses of HPV vaccine had similar likelihood to have received their providers' recommendations for a Pap test in the past 12 months.
FIG. 1.
Pap smear and provider's recommendation for Pap smear by doses of HPV vaccine, NHIS 2013–2015 (n = 1497). Young adult women with valid information on the doses of HPV vaccine received (n = 1497) were included in the analyses. HPV, human papillomavirus; NHIS, National Health Interview Survey; Pap, Papanicolaou.
The types of providers that a women visited last year modified the relationship between HPV vaccination and Pap smear use. In the past year, 35.7% only visited an OB/GYN, 17.3% visited both an OB/GYN and another provider who was not OB/GYN, 8.5% only visited a nurse practitioner/physician assistant/midwife, and 33.0% only visited another type of health provider. Among women who visited an OB/GYN in the past year, both vaccinated women and unvaccinated women had a similar likelihood of receiving a Pap smear in the past year (84.5% vs. 81.1%, p = 0.097), to receive a provider's recommendation for Pap testing (66.0% vs. 64.4%, p = 0.69), to obtain Pap testing after receiving a provider's recommendation (87.8% vs. 85.2%, p = 0.29), and to initiate Pap testing themselves without a provider's recommendation (78.2% vs. 74.2%, p = 0.22).
In contrast, among women who only visited a nurse practitioner/physician assistant/midwife in the past year, vaccinated women had a higher likelihood of receiving a Pap smear and initiating Pap smear themselves. Among women who only visited other health providers in the past year, vaccinated women had a higher likelihood of receiving a Pap smear and receiving a recommendation for a Pap smear. Furthermore, vaccinated women were more likely to receive a Pap smear whether their provider recommended it or not. When the variable of whether visiting an OB/GYN or not in the past year was introduced into the multivariate logistic regression model, the intensity of positive association between HPV vaccination and Pap smear use was reduced (adjusted prevalence ratio and its 95% CIs reduced from 1.27 [1.19–1.34] to 1.15 [1.09–1.22]).
Sensitivity analysis that excluded women who received the first dose of the HPV vaccine after 26 years of age (n = 29) showed similar results to those that included all women.
Discussion
We explored the role of providers and patients in the relationship between HPV vaccination and Pap testing among young women in the United States, and found that those who were vaccinated were more likely to receive cervical cancer screening recommendations from their healthcare providers, to obtain Pap testing after a provider's recommendation, and to initiate screening themselves even when they did not receive a provider's recommendation.
Among women who visited an OB/GYN in the past year, vaccinated women and unvaccinated women had a similar likelihood of receiving a provider's recommendation for Pap testing, to obtain Pap testing after a provider's recommendation, and to initiate Pap testing themselves without a provider's recommendation. In contrast, women who saw providers other than an OB/GYN were less likely to receive a Pap smear. This demonstrates the need for referral to an OB/GYN if that provider does not offer cervical cancer screening.
Since unvaccinated women are not protected against HPV, not receiving regular screening leaves them particularly vulnerable to developing cervical cancer. Barriers, such as personal beliefs, literacy, lack of health insurance, and limited access to care may contribute to disparities in cervical cancer prevention among unvaccinated women.27,28 Thus, greater efforts are needed to implement vaccination and screening programs to improve cervical cancer preventive care among underserved women by eliminating barriers at both provider and patient level.
Innovative vaccination delivery methods and assistance programs need to be explored to improve initiation of HPV vaccination and access to preventive care.17,29 Unvaccinated women should be encouraged to visit OB/GYN for their routine care whenever this is feasible. However, unvaccinated women had a lower socioeconomic status compared to vaccinated women, which may affect their access to preventive healthcare. Continued support and promotion of the NBCCEDP is also an important way to target disparities in Pap testing uptake, as this program provides cervical cancer screening to low-income, underserved, and uninsured women.15,16
Among unvaccinated women, over 35% of Pap smears were initiated by the women themselves, underscoring the importance of education and outreach to improve the awareness of the benefits of cervical cancer screening. Therefore, targeted educational and outreach programs may also be utilized to eliminate barriers for HPV vaccination and cervical screening in underserved women.30,31
We found overall that vaccinated women underwent Pap testing more than unvaccinated women. These results are consistent with prior studies, which found that HPV vaccination was positively associated with Pap smear uptake in young U.S. women.18,19 An U.K. study32 also found increased Pap smear uptake in vaccinated young women. In contrast, an Australian study33 found decreased cervical screening among vaccinated young women, which may be partly due to the study design (linked registries) and campaigns for catch-up vaccination delivered through schools, general practices, and community immunization services.
Using data from administrative insurance claims records, our team assessed the impact of HPV vaccine doses on adherence to cervical cancer screening guidelines and found that young women who received three doses were more likely to be screened 3 years following vaccine initiation.34 A nested case–control study in Alberta, Canada also found that vaccinated women had a higher screening rate than unvaccinated women.35 Moreover, Lash and coworkers found that women who received three doses of the HPV vaccine and were screened after 21 years of age had much higher screening rates than unvaccinated women.36
Together, these studies demonstrate that there is no adverse impact of HPV vaccination on Pap smear uptake among young adult women in the United States. Conversely, vaccination may act as a marker for women who are getting adequate care and screening, while unvaccinated women are not receiving the same level of healthcare. Recognition of disparities in screening among unvaccinated women is the first step toward improving cancer preventive care and health equity in this group.
The main strength of this study is the use of multiple years of data from NHIS, a large, nationally representative sample with high response rates and available information on sociodemographic characteristics and healthcare access. We were able to combine data from recent years to reliably estimate prevalence of Pap testing between vaccinated and unvaccinated women, and to explore potential reasons for disparities in Pap smear use.
One limitation of this study is that Pap smear use and HPV vaccination were self-reported and may subject to recall bias. We may have overestimated Pap smear use as we did not have medical records to confirm participants' reports.37–43 Validity of self-reported HPV vaccination could not be determined. Additionally, NHIS lacks data on how often providers decline a patient's request for cervical cancer screening. Furthermore, we could not make causal inferences about provider recommendations associations with HPV vaccination and cervical cancer screening due to the cross-sectional nature of this study.
Conclusions
Young women who have been vaccinated against HPV were more likely to have received a Pap smear in the past 3 years or in the past year than unvaccinated women. Vaccinated young women are more likely to receive providers' recommendations for Pap testing and to initiate screening themselves without providers' recommendations. Unvaccinated women are more vulnerable to developing cervical cancer. Recognition of disparities in screening among unvaccinated women demonstrates the need to focus on improving screening in this group, by eliminating barriers at both the provider and patient level. Assistance programs and targeted educational and outreach programs may be adopted to improve cervical cancer preventive care among underserved women.
Acknowledgments
Funders: Dr. Guo is currently supported by a research career development award (K12HD052023: Building Interdisciplinary Research Careers in Women's Health Program-BIRCWH; Berenson, PI) from the Office of Research on Women's Health (ORWH) and the Eunice Kennedy Shriver National Institute of Child Health and Human Development (NICHD) at the National Institutes of Health (NIH) and began work on this project as a postdoctoral fellow supported by an institutional training grant (National Research Service Award T32HD055163, Berenson, PI) from the NICHD of NIH. The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH.
Role of the Sponsors: All data from NHIS used in this study were collected by the National Center for Health Statistics (NCHS) of the Centers for Disease Control and Prevention (CDC). The findings and conclusions in this article are those of the author and do not necessarily represent the views of CDC/NCHS. The sponsors had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; and preparation, review, or approval of the article, and decision to submit the article for publication.
Author Disclosure Statement
No competing financial interests exist.
References
- 1.Bouvard V, Baan R, Straif K, et al. A review of human carcinogens—Part B: Biological agents. Lancet Oncol 2009;10:321–322 [DOI] [PubMed] [Google Scholar]
- 2.de Sanjose S, Quint WG, Alemany L, et al. Human papillomavirus genotype attribution in invasive cervical cancer: A retrospective cross-sectional worldwide study. Lancet Oncol 2010;11:1048–1056 [DOI] [PubMed] [Google Scholar]
- 3.Rodríguez AC, Solomon D, Herrero R, et al. Impact of human papillomavirus vaccination on cervical cytology screening, colposcopy, and treatment. Am J Epidemiol 2013;178:752–760 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Muñoz N, Manalastas R, Pitisuttithum P, et al. Safety, immunogenicity, and efficacy of quadrivalent human papillomavirus (types 6, 11, 16, 18) recombinant vaccine in women aged 24–45 years: A randomised, double-blind trial. Lancet 2009;373:1949–1957 [DOI] [PubMed] [Google Scholar]
- 5.Castellsagué X, Muñoz N, Pitisuttithum P, et al. End-of-study 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 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Garland SM, Hernandez-Avila M, Wheeler CM, et al. Quadrivalent vaccine against human papillomavirus to prevent anogenital diseases. N Engl J Med 2007;356:1928–1943 [DOI] [PubMed] [Google Scholar]
- 7.FUTURE II Study Group. Quadrivalent vaccine against human papillomavirus to prevent high-grade cervical lesions. N Engl J Med 2007;356:1915–1927 [DOI] [PubMed] [Google Scholar]
- 8.Joura EA, Giuliano AR, Iversen OE, et al. A 9-valent HPV vaccine against infection and intraepithelial neoplasia in women. N Engl J Med 2015;372:711–723 [DOI] [PubMed] [Google Scholar]
- 9.Guo F, Hirth JM, Berenson AB. Comparison of HPV prevalence between HPV-vaccinated and nonvaccinated young adult women (20–26 years). Hum Vaccin Immunother 2015;11:2337–2344 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Markowitz LE, Liu G, Hariri S, Steinau M, Dunne EF, Unger ER. Prevalence of HPV after Introduction of the Vaccination Program in the United States. Pediatrics 2016;137:1–9 [DOI] [PubMed] [Google Scholar]
- 11.Hildesheim A, Herrero R, Wacholder S, et al. Effect of human papillomavirus 16/18 L1 viruslike particle vaccine among young women with preexisting infection: A randomized trial. JAMA 2007;298:743–753 [DOI] [PubMed] [Google Scholar]
- 12.U.S. Preventive Services Task Force. The guide to clinical preventive services, 2014. Available at: www.ahrq.gov/professionals/clinicians-providers/guidelines-recommendations/guide/cpsguide.pdf Accessed August11, 2014
- 13.Saslow D, Solomon D, Lawson HW, et al. American Cancer Society, American Society for Colposcopy and Cervical Pathology, and American Society for Clinical Pathology screening guidelines for the prevention and early detection of cervical cancer. CA Cancer J Clin 2012;62:147–172 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.Committee on Practice Bulletins—Gynecology. ACOG Practice Bulletin Number 131: Screening for cervical cancer. Obstet Gynecol 2012;120:1222–1238 [DOI] [PubMed] [Google Scholar]
- 15.Lee NC, Wong FL, Jamison PM, et al. Implementation of the National Breast and Cervical Cancer Early Detection Program: The beginning. Cancer 2014;120 Suppl 16:2540–2548 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Sanders LD, Larkins TL, Boyle JN, George SF, Triplett EW, Leypoldt MD. National Breast and Cervical Cancer Early Detection Program partnerships in action. Cancer 2014;120 Suppl 16:2612–2616 [DOI] [PubMed] [Google Scholar]
- 17.Centers for Disease Control and Prevention (CDC). National and state vaccination coverage among adolescents aged 13 through 17 years—United States, 2010. MMWR Morb Mortal Wkly Rep 2011;60:1117–1123 [PubMed] [Google Scholar]
- 18.Williams WW, Lu PJ, Saraiya M, et al. Factors associated with human papillomavirus vaccination among young adult women in the United States. Vaccine 2013;31:2937–2946 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19.Sauer AG, Jemal A, Simard EP, Fedewa SA. Differential uptake of recent Papanicolaou testing by HPV vaccination status among young women in the United States, 2008–2013. Cancer Epidemiol 2015;39:650–655 [DOI] [PubMed] [Google Scholar]
- 20.Guo F, Hirth JM, Berenson AB. Effects of cardiovascular disease on compliance with cervical and breast cancer screening recommendations among adult women. J Womens Health (Larchmt) 2015;24:641–647 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Guo F, Hirth JM, Berenson AB. Cervical cancer screening among women ≥70 years of age in the United States—A referral problem or patient choice. Prev Med 2015;81:427–432 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Guo F, Kuo YF. Roles of health care providers and patients in initiation of unnecessary Papanicolaou testing after total hysterectomy. Am J Public Health 2016;106:2005–2011 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23.National Center for Health Statistics. National Health and Nutrition Examination Survey: Questionnaires, Datasets, and Related Documentation. Available at: www.cdc.gov/nchs/nhanes/nhanes_questionnaires.htm Accessed May26, 2017
- 24.Bieler GS, Brown GG, Williams RL, Brogan DJ. Estimating model-adjusted risks, risk differences, and risk ratios from complex survey data. Am J Epidemiol 2010;171:618–623 [DOI] [PubMed] [Google Scholar]
- 25.Norton EC, Miller MM, Kleinman LC. Computing adjusted risk ratios and risk differences in Stata. Stata J 2013;13:492–509 [Google Scholar]
- 26.National Center for Health Statistics. Survey Description, National Health Interview Survey, 2013. Hyattsville, MD, 2014 [Google Scholar]
- 27.Coronado GD, Thompson B, Koepsell TD, Schwartz SM, McLerran D. Use of Pap test among Hispanics and nonHispanic whites in a rural setting. Prev Med 2004;38:713–722 [DOI] [PubMed] [Google Scholar]
- 28.Akinlotan M, Bolin JN, Helduser J, Ojinnaka C, Lichorad A, McClellan D. Cervical cancer screening barriers and risk factor knowledge among uninsured women. J Community Health 2017;42:770–778 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 29.Berenson AB, Rahman M, Hirth JM, Rupp RE, Sarpong KO. A human papillomavirus vaccination program for low-income postpartum women. Am J Obstet Gynecol 2016;215:318.e311–e319 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 30.Luque JS, Tyson DM, Markossian T, et al. Increasing cervical cancer screening in a Hispanic migrant farmworker community through faith-based clinical outreach. J Low Genit Tract Dis 2011;15:200–204 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 31.Chan DN, So WK. A systematic review of randomised controlled trials examining the effectiveness of breast and cervical cancer screening interventions for ethnic minority women. Eur J Oncol Nurs 2015;19:536–553 [DOI] [PubMed] [Google Scholar]
- 32.Beer H, Hibbitts S, Brophy S, Rahman MA, Waller J, Paranjothy S. Does the HPV vaccination programme have implications for cervical screening programmes in the UK? Vaccine 2014;32:1828–1833 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 33.Budd AC, Brotherton JM, Gertig DM, Chau T, Drennan KT, Saville M. Cervical screening rates for women vaccinated against human papillomavirus. Med J Aust 2014;201:279–282 [DOI] [PubMed] [Google Scholar]
- 34.Hirth JM, Lin YL, Kuo YF, Berenson AB. Effect of number of human papillomavirus vaccine doses on guideline adherent cervical cytology screening among 19–26 year old females. Prev Med 2016;88:134–139 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 35.Kim J, Bell C, Sun M, et al. Effect of human papillomavirus vaccination on cervical cancer screening in Alberta. CMAJ 2016;188:E281–E288 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 36.Paynter CA, Van Treeck BJ, Verdenius I, et al. Adherence to cervical cancer screening varies by human papillomavirus vaccination status in a high-risk population. Prev Med Rep 2015;2:711–716 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 37.Bowman JA, Sanson-Fisher R, Redman S. The accuracy of self-reported Pap smear utilisation. Soc Sci Med 1997;44:969–976 [DOI] [PubMed] [Google Scholar]
- 38.Montaño DE, Phillips WR. Cancer screening by primary care physicians: A comparison of rates obtained from physician self-report, patient survey, and chart audit. Am J Public Health 1995;85:795–800 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 39.Suarez L, Goldman DA, Weiss NS. Validity of Pap smear and mammogram self-reports in a low-income Hispanic population. Am J Prev Med 1995;11:94–98 [PubMed] [Google Scholar]
- 40.Vernon SW, Briss PA, Tiro JA, Warnecke RB. Some methodologic lessons learned from cancer screening research. Cancer 2004;101(5 Suppl):1131–1145 [DOI] [PubMed] [Google Scholar]
- 41.Johnson CS, Archer J, Campos-Outcalt D. Accuracy of Pap smear and mammogram self-reports in a southwestern Native American tribe. Am J Prev Med 1995;11:360–363 [PubMed] [Google Scholar]
- 42.Gordon NP, Hiatt RA, Lampert DI. Concordance of self-reported data and medical record audit for six cancer screening procedures. J Natl Cancer Inst 1993;85:566–570 [DOI] [PubMed] [Google Scholar]
- 43.Caplan LS, McQueen DV, Qualters JR, Leff M, Garrett C, Calonge N. Validity of women's self-reports of cancer screening test utilization in a managed care population. Cancer Epidemiol Biomarkers Prev 2003;12(11 Pt 1):1182–1187 [PubMed] [Google Scholar]