UBC Faculty Research and Publications

Ending cervical cancer screening: attitudes and beliefs from ethnically diverse older women Sawaya, G.; Iwaoka-Scott, A.Y.; Kim, S.; Wong, S.T.; Huang, A.J.; Washington, A.E.; Perez-Stable, E.J. 2009

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1  9 October 2007 Ending Cervical Cancer Screening: Attitudes and Beliefs from Ethnically Diverse Older Women  George F. Sawaya, MD (1,2,3) A. Yuri Iwaoka-Scott, MA (1) Sue Kim, PhD, MPH (3,4) Sabrina T. Wong, RN, PhD (3,5) Alison J. Huang, MD, MPhil (3,4) A. Eugene Washington, MD, MSc (1,2,3) Eliseo J. Pérez-Stable, MD (3,4)  1 Department of Obstetrics, Gynecology and Reproductive Sciences, University of California San Francisco (UCSF) 2 Department of Epidemiology and Biostatistics, UCSF 3 Medical Effectiveness Research Center for Diverse Populations, UCSF 4 Division of General Internal Medicine, Department of Medicine, UCSF 5 University of British Columbia School of Nursing and Centre for Health Services and Policy Research, Vancouver, British Columbia, Canada Corresponding author: Eliseo J. Pérez-Stable, MD, 3333 California Street, Suite 335, San Francisco, CA 94134-0856; Phone: (415) 502-4088 Fax: (415) 502-8291; email: eliseops@medicine.ucsf.edu Text word count: 2289 Abstract word count: 250  2 ABSTRACT  Background Guidelines support ending cervical cancer screening in women aged 65 or 70 years and older with prior normal testing, but little is known about women’s attitudes and beliefs about ending screening. Methods We recruited and interviewed 199 women aged 65 years and older from primary care clinics. All had prior cervical cancer screening and no prior hysterectomy. In face-to-face interviews conducted in English, Spanish, Cantonese or Mandarin, women were asked about various aspects of cervical cancer screening and their plans to continue lifelong screening. Results Most interviewees (74.4%) were non-White (44.7% Asian, 18.1% Latina and 11.6% African-American). Most (68%) thought that lifelong screening was either important or very important, a belief held more strongly by African-American (77%) and Latina (83%) women compared to women in other ethnic groups (p<0.01); most (77%) had no plans to discontinue screening or had ever thought of discontinuing (69%). When asked if they would end screening if recommended by their physician, however, 68% responded “yes.” In multivariable analyses, older age (OR=1.25 per year; CI=1.09-1.44), having public insurance (OR=3.84; CI=1.56-9.46) and having no personal (OR=3.13; CI=1.12-8.73) or family (OR=3.06; CI=1.19-7.89) history of cancer remained independent predictors of ending screening if recommended by their physician. Conclusions The majority of these ethnically diverse women believe that lifelong cervical cancer screening is important. Many women, however, reported they would end screening if recommended by their physician, underscoring the important role of clinicians in informing women about screening guidelines designed to maximize screening benefits and minimize harms.  3 Introduction Since the widespread implementation of cytology-based cervical cancer screening, cervical cancer incidence and mortality have fallen dramatically in the United States 1. For many decades, all women were encouraged to have annual testing and efforts were directed toward increasing screening rates. Although under use of screening in certain populations remain a problem, increased enthusiasm for screening among physicians and women alike has resulted in over-screening among women at low risk for cervical neoplasia. Among low-risk women, the chance that a positive test represents true disease is substantially lower 2, 3, and false-positive testing can generate worry and trigger unnecessary and possibly harmful interventions including colposcopy, biopsy and invasive cervical treatments. In an effort to maximize screening benefits and minimize screening harms, several national organizations have examined the evidence to determine appropriate ages after which women can safely end cervical cancer screening. Citing a lack of high-quality evidence to guide screening cessation in older women, the American College of Obstetricians and Gynecologists (ACOG) recommends lifelong testing in women who have a cervix 4. The American Cancer Society (ACS), on the other hand, supports ending screening in women aged 70 years and older with 3 or more prior normal cytology tests and no abnormal cytology tests within the past 10 years 5. The US Preventive Services Task Force (USPSTF) has a stronger position and actively discourages screening in women aged 65 years and older who have had prior normal Pap testing and who are not otherwise at high risk for cervical cancer 6. The USPSTF gives this preventive service a “D” recommendation, indicating that screening this population is either ineffective or that the harms outweigh the benefits.  4 Despite the ACS and USPSTF recommendations, studies of physicians and patients conducted after release of the new guidelines indicate that most American obstetrician/gynecologists still screen low-risk women over age 65 years often and indefinitely 7, and that most women prefer lifelong screening 8. While women from ethnic minority groups have a disproportionate incidence of cervical cancer 1 and hence have been targeted to improve participation in screening programs, little is known about how older women in these groups perceive the importance of cervical-cancer screening and how they view contemporary recommendations to end screening. To address these issues, we sought to examine attitudes and beliefs on ending cervical cancer screening from an ethnically diverse group of women aged 65 years and older.  5 Methods Participants and recruitment Between October 2002 and December 2005, we interviewed women from 4 racial/ethnic groups to assess their perceived risk across three cancer prevention scenarios: a) general screening for colon cancer, b) chemoprevention of breast cancer, and c) ending cervical cancer screening. Women were randomly assigned to answer one of the 3 scenario questions, but all women older than 65 years without prior hysterectomy were assigned to answer the cervical cancer screening section; those with prior hysterectomy were given either breast or colon cancer scenarios. Women were asked during a face-to-face interview about their understanding of cancer risk, knowledge about screening, communication with their physician about screening risk and benefits, and trust in their doctor’s recommendation about cancer screening. In the current analysis, we report outcomes related only to ending cervical cancer screening. After approval from the University of California, San Francisco (UCSF) Committee on Human Research, we recruited women from 3 primary care practices at the UCSF Medical Center and community-based public clinics. Eligible women included those who were aged 50 to 80 years, who self-identified as White, Latina, African-American or Asian (mainly Chinese), and had seen a clinician at the clinical site at least once in the previous 2 years. Using these criteria, we used administrative data to generate a list of potentially eligible women. We then contacted the clinicians involved in their care and requested permission to contact their patients. We excluded women who no longer had the same physician within the participating practices and those with current cancer or with cognitive impairments identified by their physician. Personalized letters were sent to potential participants in English, Spanish or Chinese. Two weeks after the introductory letter was sent, eligible and willing participants completed a 20-  6 minute telephone-screening questionnaire in English, Spanish, Cantonese or Mandarin and were scheduled for a 60-minute face-to-face interview. Survey description The face-to-face interview included items derived from standard questions developed and used in previous surveys and from formative focus groups. The questionnaire was developed simultaneously in English, Spanish, and Chinese using bilingual research assistants and was pretested in each of the four racial/ethnic groups, specifically testing for cultural, linguistic, and literacy appropriateness. The cervical cancer screening interviews focused on risk perception, based on the Weinstein conceptual framework 9 and included the nature and probability of harm and the factors that influence individual susceptibility. Other questions included health status as measured by the Medical Outcomes Study Short Form 12v2 (2). Predictors and outcomes about cervical cancer screening We asked women questions about the importance of regular cervical cancer screening (very important, important, not important), plans to continue screening for the rest of their lives (yes/no), whether they had ever thought about not getting Pap tests any more (yes/no), and whether based on their doctor’s recommendation they would stop getting Pap tests (yes/no). Women were subsequently given quantitative estimates of benefits and harms associated with ending screening 2, 3. Women were told that about “3 out of every 10,000 65 year-old women with 3 or more normal Pap tests will get cervical cancer, but about 200 women out of 10,000 per year will be told they have an abnormal Pap test result which will turn out to be OK after further testing. The more Pap tests you get, the more likely you will be told you have an abnormal Pap test.” After providing women with this information, we asked the same questions about the importance of and plans to continue lifelong cervical cancer screening.  7 Data analysis Descriptive statistics were generated for all variables and summarized using frequency distributions. Variables and demographics were compared for differences among ethnic groups. Comparisons were made using either the chi-squared test or the Fisher’s exact test for categorical variables and analysis of variance models for continuous data. Multivariate logistic regression with forward and backward stepwise modeling was used to examine the association of demographic factors and personal characteristics with the conditional decision to end cervical cancer screening if recommended by their physician. Statistical Analysis System (SAS, version 8.2) was used to analyze data. All analyses were two-sided (alpha=0.05).  8  Results Interviews were completed by 199 women aged 65 years and older (mean age, 70.9 years) who had no prior hysterectomy and who had previous regular cervical cancer screening. Other demographic characteristics are listed in Table 1. Most interviewees (74.4%) were non-White (44.7% Asian, 18.1% Latina and 11.6% African-American), had been or were currently married, had at least a high school education and reported “good” to “excellent health. All characteristics differed significantly by ethnicity (p < 0.05), except age. We asked several questions related to screening attitudes (Table 2). Most women (68%) thought that lifelong screening was either important or very important, a belief held more strongly by African-American and Latina women compared to women in Asian and White groups (p<0.01). Over three quarters (77%) planned to be screened for the rest of their lives and about 60% had never thought of ending screening. Being provided with quantitative information about benefits and harms of continued cervical cancer screening did not change subjects’ belief that lifelong Pap testing was either important or very important (68% pre-information versus 65% postinformation) nor did it change their plans to continue screening for the rest of their lives (77% pre-information versus 77% post-information, p>0.05 for both comparisons). About two thirds (68%) of women stated they would end screening if it were recommended by their physicians. Ethnicity was a significant factor in this decision (p=0.05), and over three fourths of Asian women would accept this recommendation. Table 3 shows proportion of women responding “yes” to this question stratified by variables; women who were older, had less than a high school education, had only public insurance, were born outside of the US and/or had no personal or family history of cancer were more likely to end screening based on their physician’s  9 recommendation. Perceived risk of cervical cancer, trust in physicians and the belief that doctors should make important medical decisions, not patients, were not significant factors in this decision (Table 3). In multivariate analyses, older age, having public insurance and having no personal or family history of cancer, but not ethnicity, remained independent predictors of ending screening (Table 4). About 20% (n=40) of women reported having ever discussed discontinuing screening with their clinicians (Table 5). In bivariate analyses, these women were less likely to be married and more likely to have attained higher educational levels and report better overall health status compared to women who did not discuss discontinuing with their clinicians (p<0.05 for all; data not shown). Most conversations about ending screening were instigated by clinicians and lasted less than 5 minutes. Fewer than a quarter of these conversations included information about risks and benefits. Over half of women (n=23) who had participated in these conversations reported that their doctors recommended ending screening and, of these women, 87% (n=20) reported that they had ended screening.  10 Conclusions The majority of women in this ethnically diverse sample believed that lifelong cervical cancer screening was important; African-American and Latina women were more likely to hold this view compared to Asian and White women. Most women had no plans to discontinue screening or had never thought of discontinuing. Regardless of ethnicity, however, most women reported they would end screening if their physician recommended it. While our finding that women in older age groups and those with no personal or family history of cancer are more likely to end screening based on physician recommendation is logical, the reasons behind having public insurance being a predictor are less clear. We attempted to determine if perception of physicians played a role but were unable to demonstrate trust or beliefs about who should be making decisions as independent risk factors for ending screening. This observation may be due to factors we were not able to measure adequately or control for. While several prior studies have explored general attitudes and beliefs about cancer screening in older individuals 10, our study uniquely focused on elucidating ethnic differences in ending cervical cancer screening. Prior studies have shown that women believe cervical cancer screening is important and 75% of women have come to expect an annual Pap test 11. Current data indicate that women have mixed attitudes about risk-based screening schedules. Some studies indicate that the majority of women plan to continue cervical cancer screening indefinitely and want annual screening even if their physicians recommend otherwise 8, perhaps due to mistrust of physicians’ rationales for recommending less frequent testing 12, 13. However, in a study of younger and middle-aged, educated, White women conducted in New England, women identified patient education and clinician-patient reasons (such as feeling comfortable with the clinician and being taken seriously) as more important in the annual exam than getting a  11 Pap test, leading investigators to conclude that in that population, biennial or triennial screening would be acceptable 14. Although there is a dearth of information about older women’s attitudes about ending cervical cancer screening, some studies have revealed their attitudes about ending other types of cancer screening. Women over age 70 express a disinclination to end breast cancer screening, though they identify increasing age, poor health, and physicians’ recommendations as potential reasons for ending screening 10. Nevertheless, rates of mammography do decrease with age, as do rates of cervical cancer screening 15. Our study has both strengths and limitations. We were able to recruit a sizable group of women aged 65 and older most of whom were non-White, allowing us to compare many outcomes by ethnicity. Power to detect differences in some subgroups, however, was limited. While the setting of a structured interview allowed us to gather more complete data than a selfadministered survey, the presence of an interviewer may have influenced how some women responded. We also realize that stated beliefs may not reflect actual clinical behaviors. While part of our survey included quantitative information about risk of cervical cancer, we could not assume that women understood these risks, especially since risk were on such a small scale. Some authors have suggested that elderly patients be given quantitative information to facilitate shared informed decision making 16. Whether or not risks of such a small magnitude, such as those associated with cervical cancer incidence in low-risk older women, lend themselves to the shared informed decision-making model remains unclear. While our study indicates that many women indicate that they would indeed end screening if their physician recommended it, a substantial proportion would want lifelong testing. Recent decision analyses indicate that lifelong screening of low-risk women is not cost-effective  12 17  and is associated with harms that eclipse benefits as women age 2. Such findings support the  USPSTF guideline that encourages screening cessation in low-risk women after the age of 65 years in an effort to maximize screening benefits and minimize harms. While clinicians often respect the desires of individuals to continue lifelong screening, it is unclear if such decisions sit squarely within the purview of individual women. It may well be that low-risk women who insist on annual, lifelong screening are requesting care outside the limits of what is reasonable to offer and that other models of care should be considered (e.g., paying out of pocket for cost-ineffective services). Future studies should focus on best ways to explain the rationale behind ending cancer screening in older individuals to facilitate satisfaction with ultimate decisions.  13 Acknowledgements We would like to thank the support of Julissa Saavedra, Sonya Morrow-Johnson, Karen Lau and other interviewers who administered the survey, of Alicia Fernandez, MD for helping coordinate recruitment through the Community Clinic Network, of Albert Yu, MD for participation of the family medicine practice, Alex Li, MD for engaging the Chinatown clinic and Cecilia Populus-Eudave for overall administrative support. We are also grateful to all the primary care physicians who gave permission to allow us to contact their patients.  14 Table 1: Study participant demographic characteristics (N=199), San Francisco 2002-2005 Characteristic  Ethnicity White  African-  Total  Latina  Asian  N=199  American N=51  N=23  N=36  N=89  (25.6%)  (11.6%)  (18.1%)  (44.7%)  29 (56.9%)  10 (43.5%)  9 (25.0%)  39 (43.8%)  Age, years 65-69  87 (43.7%)  70-74  14 (27.5%)  8 (34.8%)  16 (44.4%)  34 (38.2%)  72 (36.2%)  75+  8 (15.7%)  5 (21.7%)  11 (30.6%)  16 (18.0%)  40 (20.1%)  Mean age, years  70.3 (3.8)  70.4 (3.9)  73.0 (4.3)  70.6 (4.1)  70.9 (4.1)  17 (33.3%)  5 (21.7%)  12 (33.3%)  49 (55.1%)  83  (std) Marital status Married  (41.7%) Formerly married  27 (52.9%)  16 (69.6%)  18 (50.0%)  38 (42.7%)  99 (49.7%)  Never married  7 (13.7%)  2 (8.7%)  6 (16.7%)  2 (2.3%)  17 (8.5%)  15 Education Less than high  2 (3.9%)  3 (13.0%)  25 (69.4%)  47 (52.8%)  school graduate High school  77 (38.7%)  15 (29.4%)  10 (43.5%)  8 (22.2%)  16 (18.0%)  graduate or some  49 (24.6%)  college College graduate  34 (66.7%)  10 (43.5%)  3 (8.3%)  26 (29.2%)  or graduate school  73 (36.7%)  Insurance† Public  15 (30.0%)  11 (47.8%)  26 (76.5%)  63 (74.1%)  115 (59.9%)  Private  35 (70.0%)  12 (52.2%)  8 (23.5%)  22 (25.9%)  77 (40.1%)  Health Status Poor or fair  7 (14.0%)  10 (43.5%)  21 (58.3%)  54 (60.7%)  92 (46.5%)  Good, very good  43 (86.0%)  13 (56.5%)  15 (41.7%)  35 (39.3%)  or excellent  106 (53.6%)  Income# ≤ $15,000/year  8 (17.8%)  4 (21.1%)  12 (48.0%)  26 (36.1%)  50 (31.1%)  Born in the United States  42 (84.0%)  23 (100.0%)  1 (2.8%)  5 (5.6%)  71 (35.9%)  16 Family history of  19 (38.0%)  11 (50.0%)  16 (45.7%)  21 (23.8%)  (34.3%)  cancer Personal history of  67  19 (37.3%)  4 (17.4%)  7 (19.4%)  12 (13.5%)  cancer  42 (21.1%)  p<0.05 for differences in proportions across all race/ethnicity strata except for age as a categorical variable. †excludes 7 uninsured women #based on 2003 Health and Human Services poverty guidelines for households of 3 ($15,260)  17 Table 2: Attitudes about screening indefinitely: women who have had prior screening and who have not had a hysterectomy (N=199) , San Francisco 2002-2005 Question  Ethnicity  Total  White  African-  Latina  Asian  (n=51)  American  (n=36)  (n=89)  P value  N=199  (n=23) How important to you is it to continue getting Pap tests for the rest of your life? Important or very  25  17  30  61  133/199  (50.0%)  (77.3%)  (83.3%)  (68.5%)  (67.5%)  <0.01  important* Do you plan to get Pap tests regularly for the rest of your life? Yes  37  20  28  66  151/199  (74.0%)  (90.9%)  (80.0%)  (74.1%)  (77.0%)  0.36  Have you ever thought about not getting Pap tests any more? Yes  22  4  7  28  61/199  (43.1%)  (17.4%)  (19.4%)  (32.9%)  (31.3%)  0.05  Based on your doctor’s recommendations would you stop getting Pap tests? Yes  24  13  19  63  119/199  (57.1%)  (59.1%)  (61.3%)  (78.8%)  (68.0%)  *compared to “not at all or somewhat important”  0.05  18 Table 3: Proportion of all participants answering “yes” to the question “Based on your doctor’s recommendations would you stop getting Pap tests?” (N=175*) Characteristic  Number that would end  P value  screening (%) Demographic variables Age, years 65-69  43 (55.1%)  70-74  53 (74.7%)  75+  23 (88.5%)  0.002  Marital status Married  49 (62.8%)  Formerly married  61 (73.5%)  Never married  9 (64.3%)  0.3326  Education Less than high school graduate  58 (81.7%)  High school graduate or some college  27 (57.5%)  College graduate or graduate school  34 (59.7%)  0.0057  Insurance† Public  81 (79.4%)  Private  36 (52.9%)  0.0003  Health status Poor or fair  61 (72.6%)  Good, very good or excellent  57 (63.3%)  0.1902  19 Income# ≤ $15,000/year  33 (78.6%)  >$15,000/year  61 (61.6%)  0.0508  Country of birth Born in the US  35 (56.5%)  Non US born  83 (74.1%)  0.017  Clinical history Family history of cancer Yes  31 (55.3%)  No  85 (73.9%)  0.0148  Personal history of cancer Yes  16 (47.1%)  No  103 (73.1%)  0.004  Perceptions and attitudes Perceived risk of cervical cancer No risk, very low, somewhat low or low  100 (69.0%)  Moderate, high or very high  16 (59.3%)  0.323  Agree that important medical decisions should be made by doctors, not patients+ Strongly disagree or somewhat disagree  37 (59.7%)  Somewhat agree, agree or strongly agree  82 (72.6%)  0.080  Trust in doctors to make the best medical decisions on patients’ behalf§ Not at all, a little or somewhat  20 (71.4%)  0.705  20 Mostly or completely  99 (67.8%)  *information missing for 24 participants. †excludes 7 uninsured women #based on 2003 Health and Human Services poverty guidelines for households of 3 ($15,260) +Subject agrees with the statement: “The important medical decisions should be made by doctors, not patients.” §Subject responds “mostly or completely” to the question: “How much do you trust doctors to make the best medical decisions on your behalf?”  21 Table 4: Predictors of answering “yes” to the question “Based on your doctor’s recommendations would you stop getting Pap tests?”: multivariable analysis*  Variable  Adjusted odds ratio  95% confidence interval  Age, per year  1.25  1.09-1.44  Public health insurance (vs.  3.84  1.56-9.46  No family history of cancer  3.06  1.19-7.89  No personal history of cancer  3.13  1.12-8.73  private)  *adjusted for all variables in Table 3 (race, education, marital status, income, health status, non-US born, perceived risk of cervical cancer, agree that important medical decisions should be made by doctors not patients, trust in doctors to make the best medical decisions on patients’ behalf)  22 Table 5: Women’s discussions with clinicians about not getting any more Pap tests (N=40) Variable  N (%)  Who initiated the conversation about not getting any more Pap tests? Doctor  22 (53.6%)  Patient  10 (24.4%)  Both doctor and patient  8 (20.0%)  Number of minutes talked with doctor about not getting any more Pap tests ≤ 5 minutes  34 (85.0%)  > 5 minutes  6 (15.0%)  Doctor ever discussed risks of not getting any more Pap tests  10 (23.8%)  Doctor ever discussed benefits of not getting any more Pap tests  9 (21.95%)  Doctor ever recommended stopping Pap tests  23 (57.5%)  Of these, % who actually stopped getting Pap tests *Data missing in 1 participant for each variable.  20 (87.0%)  23 References 1.  Ries LAG, Eisner MP, Kosary CL, et al., eds. SEER Cancer Statistics Review, 1975-  2002. Bethesda, MD: National Cancer Institute. 2.  Sawaya GF, Grady D, Kerlikowske K, et al. The positive predictive value of cervical  smears in previously screened postmenopausal women: the Heart and Estrogen/progestin Replacement Study (HERS). Ann Intern Med 2000;133(12):942-50. 3.  Sawaya GF, McConnell KJ, Kulasingam SL, et al. Risk of cervical cancer associated  with extending the interval between cervical-cancer screenings. N Engl J Med 2003;349(16):1501-9. 4.  ACOG practice bulletin. Cervical Cytology screening. Number 45, August 2003. Int J  Gynaecol Obstet 2003;83(2):237-47. 5.  Saslow D, Runowicz CD, Solomon D, et al. American Cancer Society Guideline for the  Early Detection of Cervical Neoplasia and Cancer. CA Cancer J Clin 2002;52:342-62. 6.  U.S. Preventive Services Task Force. Cervical cancer screening. Accessed September 5,  2007 at http://www.ahrq.gov/clinic/uspstf/uspscerv.htm. 7.  Saint M, Gildengorin G, Sawaya GF. Current cervical neoplasia screening practices of  obstetrician/gynecologists in the US. Am J Obstet Gynecol 2005;192(2):414-21. 8.  Sirovich BE, Woloshin S, Schwartz LM. Screening for cervical cancer: will women  accept less? Am J Med 2005;118(2):151-8. 9.  Weinstein ND. What does it mean to understand a risk? Evaluating risk comprehension. 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