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J Gen Intern Med. Sep 2008; 23(9): 1324–1329.
Published online May 28, 2008. doi:  10.1007/s11606-008-0633-x
PMCID: PMC2518007
NIHMSID: NIHMS46921
Preferences for Human Papillomavirus Testing with Routine Cervical Cancer Screening in Diverse Older Women
Alison J. Huang, MD, MPhil,1,2 Eliseo J. Pérez-Stable, MD,corresponding author1,2,5 Sue E. Kim, PhD,1,2 Sabrina T. Wong, RN, PhD,2,3 Celia P. Kaplan, DrPH, MA,1,2 Judith M. E. Walsh, MD, MPH,1,2 A. Yuri Iwaoka-Scott, MA,4 and George F. Sawaya, MD2,4
1Division of General Internal Medicine, Department of Medicine, University of California San Francisco, San Francisco, CA USA
2Medical Effectiveness Research Center for Diverse Populations, University of California San Francisco, San Francisco, CA USA
3University of British Columbia School of Nursing, Vancouver, BC Canada
4Department of Obstetrics, Gynecology, and Reproductive Sciences, University of California San Francisco, San Francisco, CA USA
5University of California, San Francisco, San Francisco, CA USA
Eliseo J. Pérez-Stable, Phone: +1-415-5025601, Fax: +1-415-5028291, eliseops/at/medicine.ucsf.edu.
corresponding authorCorresponding author.
Received October 18, 2007; Revised February 6, 2008; Accepted April 4, 2008.
Background
Human papillomavirus (HPV) testing is increasingly being used to determine the optimal cervical cancer screening interval in older women. Little is known about women’s attitudes toward HPV testing or how these attitudes may influence medical discussions about cervical cancer screening.
Methods
Preferences for HPV and concomitant Papanicolaou (Pap) testing were assessed through in-person interviews with diverse women aged 50 to 80 years recruited from community and university-based practices.
Results
Eight hundred and sixty-five women (257 White, 87 African American, 149 Latina, and 372 Asian) were interviewed. Approximately 60% of participants wanted to be tested for HPV and another 15% would undergo testing if recommended by their physician. Among those wanting HPV testing, 94% would want more frequent than annual Pap tests if they had a positive HPV test and a normal Pap test. Two thirds of those under age 65 would be willing to switch to triennial Pap testing, and half of those aged 65 and older would be willing to discontinue Pap testing, if they had a negative HPV test and normal Pap test. Preferences for testing varied by ethnicity, age, place of birth, and cancer history.
Conclusions
The majority of older women were willing to use HPV testing to make decisions about frequency and duration of cervical cancer screening, but up to one third would want at least annual, ongoing screening regardless of HPV test results. Efforts should be made to ensure that HPV testing is used to reinforce appropriate utilization of screening tests.
KEY WORDS: human papillomavirus, cervical cancer screening, ethnicity, Papanicolaou test
Human papillomavirus (HPV) infection is the most common sexually transmitted infection in women in the United States, with an estimated 25 million women currently infected.1 Although the majority of HPV infections are asymptomatic and resolve without consequence,2 infection with a high-risk type of HPV is a critical step in the development of cytological abnormalities that lead to cervical cancer.3 In 1999, the Food and Drug Administration (FDA) approved a DNA test for high-risk HPV types to guide the management of borderline abnormal Papanicolaou (Pap) test results; subsequently, the FDA expanded its approval to include simultaneous HPV testing with Pap testing as a primary screening strategy in women aged 30 years and older. Concurrent with several national organizations recognizing its expanded use, HPV testing is being performed with increasing frequency in the United States.4
Until recently, screening guidelines recommended documentation of at least 3 normal Pap tests before switching to less frequent than annual testing in women aged 30 years and older.5 Within the past 5 years, however, several organizations have approved routine HPV testing along with Pap testing as a substitute for requiring a series of normal Pap tests in this age group.57 Among women who are found to have both a negative HPV and a normal Pap test, current guidelines suggest waiting at least 3 years before repeating screening. Among women with a positive HPV test, several organizations continue to endorse screening women at least annually even in the setting of a normal Pap test.5,6,8
At this time, it is not clear whether routine HPV testing will lead to more or less appropriate utilization of cervical cancer screening services by women.9,10 One factor that has been shown to influence utilization of cancer screening tests in the setting of changing or conflicting guidelines is patients’ own preferences for testing.11,12 Since 1999, HPV has received increasing coverage in the media and lay press,13,14 such that women’s own concerns about HPV may be important drivers of medical discussions about screening.
We examined awareness of HPV, preferences for HPV testing, and acceptability of using HPV test results to make decisions about cervical cancer screening in a large sample of ethnically diverse older women with access to screening services. Our goal was to gain insight into the impact of HPV testing on screening decisions among older women who tend to face the most complex decisions in the face of competing medical priorities.
Setting and Sample
This study was conducted among women enrolled in the Communication of RISk Project (CRISP), a cross-sectional study designed to evaluate differences in perceptions of cancer risk among older women from 4 racial and ethnic groups (White, Latina, African American, and Asian). Between October 2002 and January 2006, women aged 50 to 80 years were recruited from continuity practices in San Francisco, including 4 primary care practices at the University of California San Francisco (UCSF) Medical Center, a community-based clinic in the Chinatown district, and the 11 Community Health Network Clinics affiliated with the San Francisco Department of Health. To be eligible, women had to be able to speak English, Spanish, Cantonese, or Mandarin, to have been seen at 1 of the practices at least once in the previous 2 years, and could not have a current diagnosis of cancer or be cognitively impaired.
Details about the process used to recruit participants in CRISP have previously been described.15 Briefly, potential participants were identified through review of administrative data from participating sites and were mailed letters informing them of the study. Trained interviewers telephoned those women who did not decline via an opt-out postcard to administer a 20-minute survey in English, Spanish, Cantonese, or Mandarin. Women participating in the telephone survey were then asked to participate in a face-to-face interview either at a UCSF research office, a clinical practice site, or their home. The institutional review boards at all sites approved the research protocol.
Questionnaire Measures
Telephone and in-person interview items were developed simultaneously in English, Spanish, Cantonese, and Mandarin using bilingual experts, and then pretested in women from each racial/ethnic group to confirm their cultural, linguistic, and literacy appropriateness. The telephone survey included questions about demographic and clinical characteristics that might influence perceptions of cancer risk or cancer screening behavior, as well as previous Pap test history.
Awareness of HPV and previous HPV testing were assessed during the in-person interview among the participants who indicated that they had not undergone hysterectomy and were therefore eligible for cervical cancer screening. Women were first asked, “Have you ever heard about human papillomavirus or HPV?” and “Have you ever had the HPV test?” Next, women were given a short introduction to the goals of HPV screening, the relationship of HPV infection to the development of cervical cancer, and the interpretation of positive and negative HPV test results (Fig. 1). This introduction did not contain specific information about existing guidelines for HPV testing or for using HPV testing to make decisions about cervical cancer screening.
Figure 1
Figure 1
Interview script that introduced participants to the principles of HPV testing. Information was presented in English, Spanish, Mandarin, or Cantonese. Interview text was pretested in all four languages before being incorporated into the study.
Women were subsequently asked, “If the HPV test was available to you, would you want to be tested?” Those women who replied “yes,” were asked, “If you had an abnormal HPV test, would you want to get Pap tests more often than once a year?” In addition, women under age 65 years who indicated that they would want to be tested were asked, “If you had a normal HPV test, along with a normal Pap test, would you be willing to get Pap tests every 3 years instead of every year?” Women aged 65 years and older who wanted to be tested were asked, “If you had a normal HPV test, along with a normal Pap test, would you be willing to stop getting Pap tests?” For all these questions, women were given the option of answering “yes,” “no,” or “if the physician recommended it.”
Data Analysis
Demographic and clinical characteristics associated with awareness of HPV and interest in obtaining HPV testing was identified using multivariable logistic regression. Among women interested in being tested for HPV, additional multivariate analyses were conducted to identify characteristics associated with preferences for more frequent Pap testing in the setting of positive and negative HPV test results. All data analyses were performed using Statistical Analysis System (SAS, version 8.2).
Participant Recruitment and Demographic Characteristics
We sent initial contact letters to 4,523 women and were unable to reach 906 (20%) because of incorrect contact information, whereas 871 (19%) were ineligible owing to language, illness, or having left the physician’s practice. A total of 1,319 completed the baseline telephone interview, of which 157 declined to participate in the second in-person interview, 2 were found to be of ineligible ethnicity, and an additional 295 had previously undergone hysterectomy and thus were not candidates for HPV or Pap testing. The remaining 865 women were included in our analysis, including 257 White, 87 African American, 149 Latina, and 372 Asian women. Demographic and clinical characteristics of participants are summarized in Table 1.
Table 1
Table 1
Demographic and Clinical Characteristics of Participants, San Francisco, 2003–2006
Awareness of and Prior Testing for HPV
Approximately one third of participants (30%, n = 252) indicated that they had previously heard about HPV, and 7% (n = 50) indicated that they had previously had the HPV test. In multivariate analysis, women were more likely to have previously heard about HPV if they were college educated or born in the United States, or if their overall health was good to excellent; they were less likely to have heard about HPV if they were older, Asian or African American (compared to White), or currently married (Table 2). Women were more likely to respond that they had previously had the HPV test if they were younger, were born in the United States, or were Latina (compared to White). There was also a borderline association with personal history of cancer (Table 2).
Table 2
Table 2
Predictors of Previous Awareness of and Testing for HPV in 865 Diverse Older Women, San Francisco, 2003–2006
Current Preferences for HPV Testing
After listening to a short introduction on the relationship of HPV to cervical cancer and the goals of HPV testing (Fig. 1), 64% of women indicated that they would want to be tested for HPV if the test were available to them, and an additional 17% indicated that they would want to be tested for HPV if the physician recommended it. The only independent predictor of interest in HPV testing in multivariable models was older age (Table 3).
Table 3
Table 3
Predictors of Preferences for More Aggressive HPV and Pap Testing in Diverse Older Women
Preferences for Pap Testing After HPV Testing
Of the 548 women who indicated that they wanted to be tested for HPV, 78% said they would want to have Pap tests more frequently than annually if they had a positive HPV test, and an additional 16% said they would agree to this if the doctor recommended it. Among women wanting more frequent Pap tests, 75% said they would want 2 Pap tests, 16% would want 3 Pap tests, and the remaining 9% would want 4 Pap tests per year. In multivariable analysis, women were more likely to desire more frequent than annual Pap testing if they were African American compared to White; there was also a borderline association with personal history of cancer (Table 3).
Among women under age 65 who indicated that they would want to be tested for HPV, 55% indicated that they would be willing to undergo Pap tests every 3 years rather than every year if they had a negative HPV test along with a normal Pap test, and an additional 12% said that they would agree to this if it were recommended by the doctor. The remaining one third of women, however, said they would want annual Pap testing in this setting. In multivariable analysis, women were more likely to want continued annual Pap testing (regardless of the doctor’s recommendation) if they were Latina compared to White, if they were born in the United States, or if their last Pap smear was less than a year ago (Table 3).
Among women aged 65 and older who wanted to be tested for HPV, approximately one third said that they would be willing to stop getting Pap tests if they had a negative HPV test in the setting of a normal Pap test, and an additional 19% said they would agree to this if it were recommended by the doctor. Nearly half indicated they would want ongoing Pap testing in the setting of a negative HPV test, regardless of the recommendation of the physician, however. No characteristics, including ethnicity, were associated with a desire for continued Pap testing in multivariable analysis (P > .05 for all).
In this study of ethnically diverse older women with access to screening, over three quarters of women said they were interested in being tested for HPV, and over 90% of women wanting to be tested said they would want more frequent Pap tests if they had a positive HPV test with a normal Pap test. In addition, two thirds of women under age 65 indicated that they would be willing to switch to triennial Pap testing if they had a negative HPV test with a normal Pap test (Table 3), and slightly more than half of those aged 65 and older indicated that they would be willing to discontinue Pap testing if they had a negative HPV test with a normal Pap test. These results suggest that a substantial proportion of older women are interested in using HPV testing to make decisions about frequency and duration of cervical cancer screening.
At the same time, our findings suggest that some older women may be reluctant to use HPV test results in a way that is clinically appropriate or consistent with current guidelines. For example, approximately a third of women under age 65 said they would not be willing to get less frequent than annual Pap tests, even if they had negative HPV and normal Pap tests, and even if their physician recommended it. Furthermore, over two thirds of women said they would want 2, 3, or 4 Pap tests per year if they had a positive HPV test with a normal Pap test, despite recommendations for annual Pap tests in this setting.
Our results are consistent with previous studies suggesting that some women are uncomfortable with stopping annual Pap testing even when advised by their physicians or confronted with evidence that annual, lifelong Pap testing offers little clinical benefit. For example, a recent telephone survey of 360 women aged 40 years and older found that 69% of women would try to continue being screened annually even if their physicians recommended less frequent screening and advised them of comparable benefits.16 Only 35% thought that there might come a time when they would stop getting Pap tests, despite national recommendations that elderly well-screened women may cease routine screening (at age 65 for the US Preventive Services Task Force, and age 70 for the American Cancer Society).5,17
Although women’s personal preferences for testing may not be the sole or even primary drivers of cancer screening practices, decisions about cancer screening in the United States are increasingly being made using a shared decision-making model.1820 Current media coverage of HPV and its relationship to cervical cancer is on the rise,13,14 and women’s interest in and attitudes toward HPV testing are likely to have an increasing impact on decision-making about cervical cancer screening.
Our findings have implications for the impact of routine HPV testing on the total volume of Pap tests performed in the United States. Over the past 2 decades, the total number of Pap tests performed on U.S. women has increased from 50 million per year to more than 65 million per year.2123 It has been estimated that the net effect of routine testing for HPV would be to reduce the total volume of Pap tests performed by 30%, or nearly 20 million per year.21 In practice, however, if up to one third of women are unwilling to forgo annual Pap testing in the setting of negative HPV and normal Pap test results, and if many women are interested in getting more frequent than annual Pap testing in the setting of positive HPV and normal Pap test results, HPV testing may not reduce overutilization of Pap testing to the extent projected unless there are other restrictions linked to payment for the test.
Our findings also provide insight into racial/ethnic and demographic differences in awareness of HPV and preferences for HPV testing in older women. In our study, women were significantly less likely to have previously heard of HPV if they were Asian or African American rather than White, if they had not graduated from college, or if they had been born outside of the United States. These findings suggest that despite increased media coverage of HPV, HPV awareness has not reached minority, immigrant, and less educated populations to the same extent as White, U.S.-born, educated women.
Furthermore, we found that older women’s decision-making about cervical cancer screening in the setting of HPV testing varied significantly by ethnicity. African American women were more likely to want more frequent than annual Pap testing after a positive HPV test, for example, and Latina women were more likely to insist on at least annual Pap testing even in the setting of a negative HPV and a normal Pap test. These trends were not explained by differences in women’s personal or family history of cancer, or other clinical characteristics such as general health status. Although a number of studies have documented racial or ethnic disparities in utilization of Pap tests,2429 there has been little research on differences in women’s personal preferences for testing by ethnicity.30,31 Further research is needed to explore possible mediators for differences in testing preferences among ethnic groups, such as differences in women’s perception of the accuracy of HPV and Pap tests, willingness to undergo more frequent procedures, and belief that more frequent testing will decrease their long-term risk of developing cancer.
Our research has several important limitations. First, this study was conducted among women in the San Francisco Bay Area, a metropolitan area that was targeted in direct-to-consumer advertising campaigns for the HPV test, and thus our results may not apply to women from other geographic regions. Second, this study was conducted between October 2002 and January 2006, before the availability of a prophylactic vaccine against HPV types 6, 11, 16, and 18. Public debate about use of the HPV vaccine may have increased public awareness of HPV and its relationship of cervical cancer, even among older women who are not currently candidates for HPV vaccination.
In addition, the CRISP study enrolled women between 50 and 80 years of age only, to focus on older women who tend to face the most complex decisions about cancer screening in the face of competing medical priorities. However, younger women are also candidates for routine HPV testing under current guidelines, and our results may not apply to this age group. Finally, this study was primarily directed at understanding women’s attitudes toward HPV testing, rather than documenting their actual testing behavior or estimating their risk of cancer. As a result, we did not try to verify women’s self-reported data about their previous Pap testing or HPV testing history by consulting their physicians or medical records, nor did we collect detailed data about clinical or behavioral factors that might influence their clinical risk of developing cancer.
Nevertheless, this study raises important questions about the impact of routine HPV testing on older women’s decision making about cervical cancer screening. If clinical guidelines are not followed, HPV testing may lead to unnecessary pap smears, increased health care expenditures, more false positive tests and additional physician visits or tests to clarify these results without any clear benefits. If HPV testing is increasingly adopted as a primary screening strategy in the United States, efforts must be made to ensure that it is used to reinforce appropriate rather than inappropriate cervical cancer screening practices.
Acknowledgments
This study was supported by the Agency for Healthcare Research and Quality (5P01 HS10856) for an Excellence Center to Eliminate Ethnic/Racial Disparities (EXCEED) and by grant P30-AG15272 under the Resource Centers for Minority Aging Research program by the National Institute on Aging, the National Institute of Nursing Research, and the National Center on Minority Health and Health Disparities, National Institutes of Health. Dr. Huang’s research efforts are further supported by Grant Number KL2RR024130 from the National Center for Research Resources, a component of the National Institutes of Health Clinical and Translational Science Award for Medical Research.
Conflict of Interest None disclosed.
Footnotes
This paper was presented at the national annual meeting of the Society for General Internal Medicine in Toronto, Canada, on April 25, 2007.
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