In 2012, the American Cancer Society, American Society for Colposcopy and Cervical Cytology, and American Society for Clinical Pathology updated their joint guidelines for cervical cancer screening, specifically recommending against annual screening using any strategy.1 Revised cervical cancer screening guidelines from the U.S. Preventative Services Task Force did not explicitly recommend against annual screening, but none of the recommended intervals after a normal screen were shorter than 3 years.2 Cytology alone at 3-year intervals and human papillomavirus (HPV) cotesting with cytology at 5-year intervals were both considered acceptable strategies for women aged 30–65 years. Although primary screening with HPV testing was not in the 2012 guidelines, in April 2014, the U.S. Food and Drug Administration approved the Roche Cobas HPV test for primary screening, and interim guidelines for a primary HPV screening strategy are anticipated.3
Human papillomavirus cotesting with a 3-year screening interval has been an acceptable option since 2003, yet uptake of cotesting in clinical practice has been slow.4,5 Studies have shown that despite these guidelines, physicians continue to screen more frequently than recommended,6–11 and surveys have indicated that patient anxiety and expectation of annual screening influence a health care provider's screening recommendation.12,13 Because recommendations strive to achieve a balance between benefits and both physical and psychological harms of screening, it is important to assess patient preferences and attitudes toward each alternative cervical cancer screening strategy.
We assessed the attitudes toward HPV testing strategies and patient-specific factors associated with willingness to lengthen screening intervals to 3 or 5 years in a cohort of routinely screened women participating in a natural history study of HPV infection during the menopausal transition.
MATERIALS AND METHODS
A survey to assess knowledge of the cervical cancer screening guideline changes, current screening practices, preferred screening method and frequency, willingness to extend the screening interval, and perceived risk of HPV and cervical cancer was offered to all women completing the HPV in Perimenopause Study final study visit. Five hundred sixty-six of 885 women enrolled into the HPV in Perimenopause Study (64.0%) completed the final study visit, and 551 of 566 (97.3%) completed the screening-focused survey. Women who completed the full 2 years of follow-up did not differ significantly on any of the demographic or baseline risk factor variables from the total 885 women enrolled (Table 1).
Details of the HPV in Perimenopause Study have been reported elsewhere.14,15 In brief, women receiving routine gynecologic care were recruited to participate from Johns Hopkins Hospital-affiliated outpatient obstetrics and gynecology clinics in Baltimore, Maryland, from March 2008 to March 2011. Women were eligible to participate in the study if they were between 35 and 60 years of age, had an intact cervix, and were willing to provide informed consent. Women were not eligible for enrollment into the study if they were pregnant, had plans to become pregnant, had a history of organ transplantation, or were known to be human immunodeficiency virus-positive.
During this 2-year prospective natural history study of HPV infection in the menopausal transition, consenting women provided information on sociodemographic characteristics, lifetime sexual history and current sexual behavior, cervical cancer screening history, menstrual and reproductive histories, medication, and alcohol and tobacco use through a telephone-administered questionnaire. All women underwent a speculum-assisted pelvic examination with swab and secretion samples collected for research purposes. A Health Insurance Portability and Accountability Act waiver was signed allowing the study to abstract all cervical cytology and HPV test results obtained clinically during their study participation from their medical records. Several patient-specific factors evaluated in this study (including screening history, sexual behavior, and clinical Pap–HPV test results) were derived from these data sources. The questions asked of participants in the screening study are included in the Appendix, available online at http://links.lww.com/AOG/A601. All study procedures were approved by the Johns Hopkins Bloomberg School of Public Health institutional review board.
Descriptive statistics including frequencies and proportions and their corresponding confidence intervals (CIs) were estimated to summarize survey responses. Poisson regression with robust error variance was used to estimate unadjusted prevalence ratios and corresponding 95% CIs comparing women willing to be screened every 3 years (by Pap only or by Pap–HPV cotesting) with women unwilling to extend screening intervals beyond 1 year. Women willing to extend screening to every 5 years after a dual negative cotest were also compared with women only willing to extend to 3 years. Women preferring Pap testing only were compared with women preferring HPV testing only or who did not express a preference. All analyses were carried out in Stata 13.1.
The women in this analysis were between 36 and 62 years of age with a median age of 50 years (interquartile range 44–55) at the time of the screening survey administration. The majority of women were white (76.2%), married (64.7%), and currently nonsmokers (91.8%) (Table 1). Many women (60.9%) reported having five or more lifetime sex partners and at the time of the final visit, 70.0% reported sex with a steady partner, 25.5% were not sexually active, and 4.6% reported having a new sex partner in the prior 6 months. Most participants had some education beyond high school (85.0%) with 64.6% completing college, a postgraduate degree, or both and 80.1% reported household incomes of $40,000 or higher. Consistent with our planned recruitment from women attending routine obstetrics and gynecology visits, all women reported having had a prior Pap test, 47.2% reported having an abnormal Pap test result before study enrollment, and 99% reported having had a Pap test within the previous 3 years. In addition to obstetrics and gynecologic care, participants were actively engaged in other medical care—fewer than 1% of women reported that their obstetrician–gynecologist was their primary care physician, and 97.6% had undergone a checkup or physical in the previous 5 years (Table 2). Additionally, 92.2% of women reported having cholesterol tests, 75.1% diabetes screens, and 88.4% mammograms in the previous 5 years.
A majority of participants (55.6%, 95% CI 51.4–59.8) were aware that current cervical cancer screening guidelines recommended against annual screening (Table 2). However, when asked how often they thought women their age should have a Pap test, 3.8% (95% CI 2.5–5.8) reported more than once a year, 74.1% (95% CI 70.3–77.7) reported yearly, 13.4% (95% CI 10.8–16.6) reported every other year, and 6.4% (95% CI 4.6–8.7) reported every 3 years or longer. Despite a majority's believing that screening should occur annually, more than two thirds of participants (68.4%, 95% CI 64.4–72.2) were willing to extend their screening to once every 3 years by either Pap test only or Pap–HPV cotesting after a normal result if a doctor recommended it; however, among those women willing to be screened every 3 years, only 39.5% (95% CI 34.5–44.7), which was 25.2% (95% CI 21.8–29.0) of women overall, were willing to extend screening to 5 years. More than two thirds of participants (69.7%, 95% CI 65.7–73.4) indicated that they would continue annual obstetrics and gynecology well-woman visits even if Pap screening was not performed. This proportion remained unchanged when restricted to the women willing to be screened every 3 years or longer. Primary reasons cited for continuing annual visits included a desire for routine checkup or physical examination, other gynecologic concerns, breast examinations, to maintain relationships with their doctor, and reassurance that everything is okay.
When asked about screening test preference, 60.7% (95% CI 56.5–65.7) of women preferred Pap tests only, 31.5% (95% CI 27.7–35.5) did not have a preference and were willing to be screened by either Pap or HPV testing, and only 7.8% (95% CI 5.9–10.4) preferred HPV testing alone (Table 2). Furthermore, 30.1% (95% CI 26.4–34.1) of women reported they would experience moderate anxiety and 11.3% (95% CI 8.9–14.3) reported severe anxiety if they were screened with an HPV test alone. When asked which test result they found more concerning, 26.6% (95% CI 23.0–30.4) said an abnormal Pap test result and 9.3% (95% CI 7.1–12.0) reported an HPV-positive test result, with the majority reporting them to be equally concerning. To understand factors associated with screening assay preference, univariate analyses compared women who preferred Pap testing alone with the women who did not have a preference or preferred HPV testing (Table 3). Women with a higher household income (prevalence ratio 0.6, 95% CI 0.5–0.9), women recruited from the clinic that routinely cotests (prevalence ratio 0.8, 95% CI 0.7–0.9), women who were more concerned about an HPV-positive test result (prevalence ratio 0.5, 95% CI 0.3–0.7) or equally concerned about an abnormal Pap–HPV test result (prevalence ratio 0.7, 95% CI 0.7–0.8), or thought they had a moderate or high risk of HPV (prevalence ratio 0.7, 95% CI 0.5–0.9) were more likely to not have a test preference or to prefer HPV-only testing compared with preferring Pap-only testing. Women with moderate (prevalence ratio 1.5, 95% CI 1.3–1.9) or severe (prevalence ratio 1.4, 95% CI 1.1–1.8) concern about HPV-only testing preferred Pap-only testing compared with women with low or no concern about HPV-only testing.
In univariate analyses, we saw little to no difference in willingness to be screened every 3 years compared with annually by age, race, marital status, education, and menopausal status (Table 4). Women with household income below $40,000 were 30% more likely (prevalence ratio 1.3, 95% CI 1.1–1.5) to agree to extended screening intervals than women with higher income. Women seen at clinic B (which instituted a clinic-wide cotest policy in 2009) were more likely to agree to extended intervals (prevalence ratio 1.2, 95% CI 1.1–1.4) compared with women recruited from clinic A, which did not have a consensus cotesting policy. Participants' knowledge and attitudes toward cervical cancer screening as well as self-reported screening history were among the strongest predictors of whether a woman was willing to be screened every 3 years. Both women who had last been screened more than 1 year previously (prevalence ratio 1.3, 95% CI 1.2–1.5) and those who did not expect to have their next Pap screening for at least 1 year (prevalence ratio 1.4, 95% CI 1.2–1.5 next screen within 2 years; prevalence ratio 1.4 95% CI 1.1–1.7 next screen within 5 years) were 30–40% more likely to agree to a 3-year screening interval. Women who believed Pap tests should be done every other year (prevalence ratio 1.3 95% CI 1.2–1.5) or every 3–5 years (prevalence ratio 1.5, 95% CI 1.4–1.7) were also significantly more likely to state they would accept extended screening intervals than those who thought screening should be yearly or more often. Prior knowledge of the change in screening guideline was not associated with an increased willingness to follow the new guidelines. Women with a history of abnormal Pap test results in the previous 5 years were at least 30% less likely to agree to extended intervals (prevalence ratio 0.7, 95% CI 0.5–0.9 extend to 3 years; prevalence ratio 0.5, 95% CI 0.2–1.0 extend to 5 years). Women who reported a moderate to high perceived risk of developing cervical cancer in the future were 30% less willing to extend screening intervals to 3 years (prevalence ratio 0.7, 95% CI 0.6–0.9), but no association was seen with perceived risk of HPV infection or genital warts. Risk factors for HPV infection and cervical cancer such as lifetime number of sex partners, recent new sex partners, HPV serology status, and HPV DNA status were also not associated with a woman's willingness to follow the 3-year screening recommendation.
Only 39.5% (95% CI 34.5–44.7) of women willing to be screened every 3 years (25.2%, 95% CI 21.8–29.0 of all women) were willing to be screened every 5 years (Table 4). Women with body mass indexes (calculated as weight (kg)/[height (m)]2) higher than 30 were 50% more likely to accept a 5-year interval (prevalence ratio 1.5, 95% CI 1.1–2.0). Many of the same determinants of willingness to extend to 3-year intervals were associated with willingness to extend to 5-year intervals, although these associations did not reach statistical significance in this smaller sample. No significant associations were seen with risk factors of lifetime number of sex partners, new sex partners, HPV serology status, and HPV DNA status.
Cervical cancer screening has evolved significantly in the past 10–15 years. However, the preference of women regarding alternative screening strategies is an understudied aspect of changing screening guidelines. In our survey of routinely screened women 36–62 years of age, we found that almost half were aware that screening recommendations had changed, and the majority still believed women should be screened every year. Despite this, two thirds stated that they would be willing to extend screening to every 3 years if their doctor recommended it, but only one fourth were willing to extend the interval to 5 years after a dual negative cotest, the preferred recommendation in the newest guidelines. Women also expressed a clear preference for Pap testing over HPV testing, and many expressed concern over having an HPV test alone without a Pap test. A desire for more frequent care, higher anxiety, and higher perceived risk were all associated with being less willing to accept alternatives to annual Pap tests.
Resistance to less frequent screening has been reported previously,16–23 and this reticence appears to persist over time. For example, the results from a nationally representative survey of women in the United States in 2005 were strikingly similar to our survey results collected almost a decade later.17 Our results suggest a continued preference for cytology testing compared with HPV testing. This observation is especially relevant in light of the recent U.S. Food and Drug Administration approval of one HPV test (Roche Cobas) for an indication of primary cervical cancer screening.3 Future U.S. guideline revisions are likely to consider recommendations for primary screening using HPV testing, especially given the transition to primary HPV screening by other large national screening programs such as those in Australia24 and the United Kingdom.25
Interestingly, despite the preference for Pap over HPV testing, women in our study were more concerned about an abnormal Pap test compared with a positive HPV test. Data from a large study of women routinely screened with an HPV cotest algorithm showed 35% of cervical intraepithelial neoplasia and adenocarinoma in situ and 29% of total cancers were in women with HPV-positive and cytology-negative cotest results.26 Taken together, these results suggest that educational interventions to communicate risks associated with alternative screening test results are needed for women to make and understand alternative screening choices.
Women with a lower household income were more likely to accept longer screening intervals, which may be related to the cost-saving aspect of reducing unnecessary tests or other barriers such as difficulty scheduling time off work for preventive health care needs. In addition, women with high levels of worry, high perceived risk, or both as well as women who indicated a preference for more care and contact with their health care provider were less likely to agree to extended screening intervals, as previously shown.16,27 These women may represent a combination of those with historically high risk, who should be screened more frequently,28 as well as a subset of “worried well” in whom frequent screening appears to be the result of a desire for continual reassurance.
Surveys of physicians have indicated that concern about losing the well-woman annual clinical encounters as a result of less frequent screening was a common barrier to use of cotesting strategies, which are cost-effective only when performed at the recommended extended intervals.10,29 It is important to understand whether a lack of willingness to extend the cervical cancer screening interval reflects a concern among the patients about missing other opportunities for care. We found that nearly 70% of women reported that they would continue annual well-woman visits even if Pap testing was not done at each visit. However, our questions did not explicitly ask about willingness to extend screening intervals in the context of continued annual gynecologic examinations and thus it is possible that acceptance would be higher if women are reassured that less frequent screening would not result in less frequent general gynecologic care.
A unique strength of our analysis was the ability to nest responses into a larger and more comprehensive evaluation of the natural history of HPV infection. For example, women in this study were primarily recruited from two gynecology practices, which had distinctly different screening policies. We observed that women recruited from the clinic with a practice-wide policy of routine cotesting in women older than 30 years since 2009 were slightly more likely to accept extended intervals than those being screened in the other clinics with less frequent use of cotesting. However, having had one or more HPV tests or being in the clinic with a policy of routine cotesting was not associated with a woman being more comfortable with HPV-only testing, again highlighting a need for more patient education regarding the use and meaning of HPV testing.
A limitation of this cohort is that it is not representative of the general population. Our study participants are older, of higher socioeconomic status, and are in routine screening. Despite this, we believe that the responses from this population are particularly relevant when the aim is to examine the attitudes toward changes in routine screening guidelines, because it is the well-screened women who would be most affected by extension of screening intervals. Moving forward, it will be important to assess whether more diverse or representative populations also express similar attitudes toward screening strategies. We also acknowledge that screening involves a dialog between the patient and health care provider, and we have only provided the patient perspectives. Future studies incorporating both patient and health care provider perspectives will be essential for a complete evaluation of the dynamics of this shared decision-making. In addition, many of the questions were phrased as screening intentions and future behaviors, and it is thus unclear whether these intentions will directly translate to practice. All of the information collected in our questionnaire are self-reported and so are subject to inaccuracies in recall and reporting. Despite these limitations, these data contribute to a significant gap in the evidence regarding patient perceptions of benefits and harms of screening, which have been historically underrepresented in cervical cancer screening guideline development.
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