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Specialty Differences in Primary Care Physician Reports of Papanicolaou Test Screening Practices: A National Survey, 2006 to 2007 FREE

K. Robin Yabroff, PhD; Mona Saraiya, MD; Helen I. Meissner, PhD; David A. Haggstrom, MD, MAS; Louise Wideroff, PhD; Gigi Yuan, MS; Zahava Berkowitz, MSc, MSPH; William W. Davis, PhD; Vicki B. Benard, PhD; and Steven S. Coughlin, PhD
[+] Article and Author Information

From the National Cancer Institute and the National Institutes of Health, Bethesda, and Information Management Services, Silver Spring, Maryland; Centers for Disease Control and Prevention, Atlanta, Georgia; Veterans Affairs Medical Center, Regenstrief Institute, and Indiana University School of Medicine, Indianapolis, Indiana; and Department of Veterans Affairs, Washington, DC.


Disclaimer: The findings and conclusions in this report are those of the authors and do not necessarily represent the views of the National Cancer Institute or the Centers for Disease Control and Prevention. Dr. Yabroff had full access to all of the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.

Acknowledgment: The authors thank the Principal Investigator, National Survey of Primary Care Physicians' Recommendations & Practice for Breast, Cervical, Colorectal, & Lung Cancer Screening; Dr. Carrie Klabunde, National Cancer Institute, for coordination and leadership of this effort and thoughtful comments on an earlier version of the manuscript; and Dr. Caroline McLeod, Westat, for survey research work.

Grant Support: By the National Cancer Institute (contract N02-PC-51308), Centers for Disease Control and Prevention (interagency agreement Y3-PC-6017-01), and Agency for Healthcare Research and Quality (interagency agreements Y3-PC-5019-01 and Y3-PC-5019-02).

Potential Conflicts of Interest: None disclosed.

Reproducible Research Statement:Study protocol: Available from Dr. Yabroff (e-mail, yabroffr@mail.nih.gov). Statistical code: Not available. Data set: Certain portions of the analytic data set are available to approved individuals through written data use agreements with the research sponsor; contact Dr. Klabunde (e-mail, klabundc@mail.nih.gov).

Requests for Single Reprints: K. Robin Yabroff, PhD, MBA, Health Services and Economics Branch/Applied Research Program, Division of Cancer Control and Population Sciences, National Cancer Institute, Executive Plaza North, Room 4005, 6130 Executive Boulevard, Bethesda, MD 20892-7344; e-mail, yabroffr@mail.nih.gov.

Current Author Addresses: Dr. Yabroff: Health Services and Economics Branch/Applied Research Program, Division of Cancer Control and Population Sciences, National Cancer Institute, Executive Plaza North, Room 4005, 6130 Executive Boulevard, MSC 7344, Bethesda, MD 20892-7344.

Drs. Saraiya and Benard and Ms. Berkowitz: Centers for Disease Control and Prevention, 4770 Buford Highway, Mailstop K-55, Atlanta, GA 30341.

Dr. Meissner: Office of Behavioral and Social Sciences Research, Office of the Director, National Institutes of Health, 31 Center Drive, Building 31/Room B1C19, Bethesda, MD 20892-2027.

Dr. Haggstrom: Veterans Affairs Health Services Research & Development Center for the Implementation of Evidence-Based Practice, 1481 West 10th Street, Indianapolis, IN 46202.

Dr. Wideroff: 6001 Executive Boulevard, National Institute on Drug Abuse, Bethesda, MD 20892.

Ms. Yuan: Information Management Services, 12501 Prosperity Drive, Suite 200, Silver Spring, MD 20904.

Dr. Davis: Social Security Administration, 6401 Security Boulevard, Baltimore, MD 21235.

Dr. Coughlin: Department of Veterans Affairs, 810 Vermont Avenue NW, Washington, DC 20420.

Author Contributions:Conception and design: K.R. Yabroff, M. Saraiya, H.I. Meissner, D.A. Haggstrom, L. Wideroff, Z. Berkowitz, S.S. Coughlin.

Analysis and interpretation of the data: K.R. Yabroff, M. Saraiya, H.I. Meissner, D.A. Haggstrom, L. Wideroff, G. Yuan, Z. Berkowitz, W.W. Davis, S.S. Coughlin.

Drafting of the article: K.R. Yabroff, M. Saraiya, H.I. Meissner, V.B. Bernard, S.S. Coughlin.

Critical revision of the article for important intellectual content: K.R. Yabroff, M. Saraiya, H.I. Meissner, D.A. Haggstrom, L. Wideroff, Z. Berkowitz, V.B. Bernard, S.S. Coughlin.

Final approval of the article: K.R. Yabroff, M. Saraiya, H.I. Meissner, D.A. Haggstrom, L. Wideroff, G. Yuan, W.W. Davis, V.B. Bernard, S.S. Coughlin.

Statistical expertise: K.R. Yabroff, W.W. Davis.

Administrative, technical, or logistic support: Z. Berkowitz.


Ann Intern Med. 2009;151(9):602-611. doi:10.7326/0003-4819-151-9-200911030-00005
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Background: Cervical cancer screening guidelines were substantially revised in 2002 and 2003. Little information is available about primary care physicians' current Papanicolaou (Pap) test screening practices, including initiation, frequency, and stopping.

Objective: To assess current Pap test screening practices in the United States.

Design: Cross-sectional survey.

Setting: Nationally representative sample of physicians during 2006 to 2007.

Participants: 1212 primary care physicians.

Measurements: The survey included questions about physician and practice characteristics and recommendations for Pap screening presented as clinical vignettes describing women by age and by sexual and screening histories. A composite measure—guideline-consistent recommendations—was created by using responses to vignettes in which major guidelines were uniform.

Results: Most physicians reported providing Pap tests to their eligible patients (91.0% [95% CI, 89.0% to 92.6%]). Among Pap test providers (n = 1114), screening practices, including number of tests ordered or performed, use of patient reminder systems, and cytology method used, varied by physician specialty (P < 0.001). Although most Pap test providers reported that screening guidelines were very influential in their clinical practice, few had guideline-consistent recommendations for starting and stopping Pap screening across multiple vignettes (22.3% [CI, 19.9% to 25.0%]). Guideline-consistent recommendations varied by specialty (obstetrics/gynecology, 16.4%; internal medicine, 27.5%; and family or general practice, 21.1%). Compared with obstetricians/gynecologists, internal medicine specialists and family or general practice specialists were more likely to have guideline-consistent screening recommendations (odds ratio, 1.98 [CI, 1.22 to 3.23] and 1.45 [CI, 0.99 to 2.13], respectively) in multivariate analysis.

Limitation: Physician self-report may reflect idealized rather than actual practice.

Conclusion: Primary care physicians' recommendations for Pap test screening are not consistent with screening guidelines, reflecting overuse of screening. Implementation of effective interventions that focus on potentially modifiable physician and practice factors is needed to improve screening practice.

Primary Funding Source: National Cancer Institute, Centers for Disease Control and Prevention, and Agency for Healthcare Research and Quality.

Editors' Notes
Context

  • The American College of Obstetrics and Gynecology, American Cancer Society, and U.S. Preventive Services Task Force modified their cervical cancer screening guidelines in the early 2000s to reflect new information about human papillomavirus and decreased the advised frequency of screening in some risk groups.

Contribution

  • In 2006 to 2007, physician responses to clinical vignettes for which all guidelines agreed suggest that fewer than 25% reported guideline-consistent care. Most variations indicated overuse of screening. Guideline-consistent responses were most frequent among internists, followed by family physicians and then gynecologists.

Caution

  • Results are not based on actual practice behaviors.

Implication

  • Physicians need to better understand cervical cancer screening recommendations.

—The Editors

In 2008, approximately 11 000 women in the United States received a diagnosis of invasive cervical cancer, and nearly 4000 women died of the disease (1). Although Papanicolaou (Pap) test screening, an evaluation of cervical cells for abnormalities for early detection of cervical cancer, is widely used (24), some women have never or rarely been screened (5). Others continue to be screened even after they are no longer at risk for cervical cancer (for example, those who had hysterectomy for benign disease) (67). Although many patient factors are associated with screening (2, 89), physician recommendation is one of the strongest predictors of cervical cancer screening (1011). By recommending such preventive services as Pap test screening to their patients, primary care physicians play a central role in implementing the screening guidelines of major professional organizations.

During 2002 and 2003, cervical cancer screening guidelines for prevention and early detection of cervical cancer were substantially revised to reflect increased understanding of the natural history of human papillomavirus (HPV) infection and its role in the development of cervical cancer, as well as to reflect the introduction of new screening methods, including liquid-based cytology (1214). Revised guidelines addressed the ideal age for starting routine Pap test screening and appropriate intervals between screening tests and identified situations when routine Pap testing should be stopped (Table 1). To assess the effect of these revisions, the National Cancer Institute, in collaboration with the Centers for Disease Control and Prevention and the Agency for Healthcare Research and Quality, conducted a national cross-sectional survey of primary care physicians about current cervical cancer screening recommendations and practices.

Table Jump PlaceholderTable 1.  Comparison of Guidelines in 2002 and 2003 for Pap Testing for Cervical Cancer
Survey Procedures

We used the American Medical Association (AMA) Physician Masterfile as the sampling frame to identify a nationally representative sample of primary care physicians. The Masterfile contains demographic and practice-related data on physicians independent of AMA membership. Physicians who were younger than 76 years, held an active license, and listed patient care as their major professional activity were eligible. We excluded physicians who were retired, in residency training, teaching, or in research or administration full-time. We selected physicians practicing in general practice, family practice, general internal medicine, and obstetrics/gynecology (OB/GYN), using a stratified random sample with the 4 specialties as the sampling strata. Selection was proportional to the specialty's representation in the U.S. physician population. The survey was administered by the contract research firm, Westat (Rockville, Maryland), and approved by the institutional review board of Westat, as well as by the U.S. Office of Management and Budget. The protocol was reviewed by the National Institutes of Health Office of Human Subjects Research and considered exempt by the National Institutes of Health institutional review board.

The primary care physician survey of cervical cancer screening was part of a larger effort to obtain current national data on physicians' knowledge, attitudes, recommendations, and practices related to screening for breast, cervical, colorectal, and lung cancer (15). Because of the need for a brief survey instrument and the complexity of the different screening technologies for each case of cancer, we used a split-sample design in which half of the participants were randomly assigned the breast and cervical cancer screening questionnaire and the other half were assigned the colorectal and lung cancer screening questionnaire.

To provide national estimates of physicians' breast and cervical cancer screening practices with a margin of error of ±3% at a 95% CI for the 4 specialties, Westat researchers identified 2567 physicians (Appendix Figure). Physicians who requested that the AMA not release their contact information (“no contact” physicians; n = 92) were included in the sample to develop accurate sample weights, but they were not surveyed. Westat researchers screened the remaining 2475 physicians to exclude those who had retired or died, no longer practiced, or could not be located (n = 527). In September 2006, the remaining 1948 eligible physicians were sent a package containing the survey instrument, a cover letter describing the study and emphasizing the importance of participation, a fact sheet, a letter of support from the physician's specialty organization (American College of Obstetrics and Gynecology, American College of Physicians, or American Academy of Family Physicians), a postage-paid return envelope, and a $50 honorarium. A second mailing was sent approximately 3 weeks later to physicians who had not yet returned their questionnaires, and follow-up calls were made shortly after the second mailing. Additional follow-up was continued through March 2007.

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Appendix Figure.
Identification of primary care physician sample.

AMA = American Medical Association.

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Measures

The survey included questions about demographic and primary care practice characteristics and knowledge, attitudes, recommendations, and practices related to use of established and emerging technologies for cervical cancer screening (16). The survey questions were cognitively tested in physicians before fielding. We selected measures of physician and practice characteristics that have been shown elsewhere to be associated with practice patterns, and we identified other novel measures that we hypothesized were associated with reported screening practice.

Physician characteristics were age, sex, race, board certification, medical school affiliation, and specialty. Because of the small number of general practice physicians (n = 50) and the similarities in screening behaviors identified here and in other studies of cancer screening (17), we combined general practice and family physicians in our analyses. Practice characteristics measured were urban or rural designation, region of the country, practice type, and percentage of uninsured and female patients seen in practice.

We measured Pap test screening practices by the volume of Pap tests ordered or performed per month, working with a nurse practitioner or physician assistant, recent continuing medical education credit earned on cervical cancer screening, and most common cytology method used (liquid-based, conventional, or other method). We also assessed implementation of cervical cancer screening guidelines in the practice and patient or physician reminders for screening in the primary care practice. Because we were interested in the systematic use of reminders, we did not classify responses of verbal prompt at office visit or looking up in the medical record at the time of visit as being either a patient or a physician reminder.

Screening beliefs included opinions about the effectiveness of the conventional Pap test and liquid-based cytology in reducing cancer mortality and whether screening guidelines from the U.S. Preventive Services Task Force, American Cancer Society, American College of Obstetricians and Gynecologists, American Academy of Family Physicians, or American College of Physicians were influential on their clinical practice.

We assessed Pap test screening recommendations with clinical vignettes related to Pap test screening initiation, frequency, and stopping. Each vignette included the woman's age, sexual history, and Pap test screening history (performed by the physician). Health status information was included in several vignettes. For each vignette, physicians were asked to recommend Pap screening for the patient at a routine office visit with Pap test annually (at least for the first 3 years), Pap test every 2 years, Pap test every 3 years, Pap test more than every 3 years, no Pap test, or other.

Guideline-consistent screening recommendations were defined for clinical vignettes in which the major screening guidelines were uniform at the time of the survey (Table 1). Two vignettes described the screening initiation of 18-year-old women presenting for their first gynecologic visit: One had never had sexual intercourse, and the other first had sexual intercourse 3 years ago. Guideline-consistent responses for these 2 vignettes were no Pap screening and Pap screening at least every 3 years, respectively. For the scenario describing the 18-year-old who first had sexual intercourse 3 years ago, responses of Pap annually, at least for the first 3 years, every 2 years, and every 3 years were considered to be guideline-consistent. The third vignette described a 35-year-old woman whose cervix was removed the previous year during hysterectomy for symptomatic fibroids and who had no history of dysplasia and 3 consecutive negative Pap test results. All guidelines recommend stopping Pap testing. The fourth vignette described a 66-year-old woman with unresectable non–small-cell lung cancer (NSCLC) who had 3 consecutive negative Pap test results. Median survival for a patient with unresectable NSCLC is generally measured in months, and because no benefits of screening could be realized, we considered a recommendation of no Pap test to be consistent with good clinical practice. To reflect the diversity of practice, including recommendations for starting and stopping Pap testing, we created a composite measure for all 4 vignettes as guideline-consistent (yes or no), and we used this measure as an outcome variable in multivariate analyses.

Statistical Analysis

We calculated the proportion of physicians providing Pap testing and restricted the sample to these physicians for the remainder of analyses. We compared physician and practice characteristics, screening practice, and beliefs by physician specialty by using chi-square statistics. We used logistic regression analyses to assess the association among physician characteristics, practice characteristics, and beliefs about screening and guideline-consistent screening recommendations. For the preliminary models, we selected a priori a core set of variables that have been shown to be associated with practice patterns. In addition to physician specialty, these variables included age, sex, board certification, and medical school affiliation (1723). We included this core set of variables in all multivariate models. We also evaluated more novel physician and practice characteristic predictor variables, which we hypothesized to be associated with screening practice but had not extensively studied. To aid in further hypothesis generation, we explored associations with these more novel variables adjusted for the a priori covariates, using a P value–driven approach to develop the final model. Variables with a statistically significant association with the outcome variable at a P value less than 0.100 were retained. We did not assess interactions between covariates.

We used the sample weight assigned to each survey respondent, accounting for the probability of selection, as well as adjustment for nonresponse by sample strata. Nonresponse adjustments were done with the branching algorithm CHAID (Chi-square Automatic Interaction Detection) and were based on variables available from the AMA Physician Masterfile for both respondents and nonrespondents. We used the statistical software SUDAAN (24) to apply the sampling weights and incorporate the stratified survey design in the descriptive statistics and logistic regressions.

Role of the Funding Source

This work was performed by federal researchers at the National Cancer Institute and the Centers for Disease Control and Prevention in consultation with an outside clinician. The survey was performed under a contract with Westat supported by the National Cancer Institute, Centers for Disease Control and Prevention, and Agency for Healthcare Research and Quality.

A total of 1212 physicians completed the survey, for a cooperation rate of 73.4%. The response rate, calculated according to a standard formula (RR3) approved by the American Association for Public Opinion Research (25) (including the “no contact” physicians in the denominator), was 67.5%. Overall, 91.0% (95% CI, 89.0% to 92.6%) of primary care physicians reported providing Pap testing as a service to their eligible patients. For the remainder of our analyses, we restricted the sample to these primary care physicians (n = 1114). Most were male and non-Hispanic white (Table 2). Most were board-certified and practiced in urban areas in a variety of settings, including solo practice (25%), single-specialty group practice (48%), and multispecialty group practice (25%). Most had a majority female patient population. Many of these characteristics varied by specialty.

Table Jump PlaceholderTable 2.  Pap Test Screening Practice and Beliefs, by Physician Specialty
Practice Characteristics and Beliefs About Pap Test Screening

We observed statistically significant variation in practice characteristics and beliefs about Pap screening by specialty (Table 2). More than 75% of OB/GYNs ordered or performed more than 40 Pap tests per month, compared with 5.2% of internists and 12.7% of general or family practice physicians (P < 0.001). They were also more likely than internists or general or family practice physicians to use patient reminders (P < 0.001). Among physicians who used patient reminders, 75.8% used mailed reminders and 39.3% used telephone reminders. Less than half of Pap test providers reported using physician reminders; among this group, 57.0% used chart reminders and 51.6% used computer prompts.

Most physicians usually used liquid-based cytology, although this varied across specialty (P < 0.001). This practice was also reflected in the high proportions of all physicians who endorsed liquid-based cytology as being very effective in reducing cancer mortality compared with the proportion who endorsed conventional Pap tests as being very effective. More than 80% of all physicians reported that at least 1 set of screening guidelines was very influential on their clinical practice, and they rated their own society guidelines higher than other society guidelines. Fewer than 2% of physicians reported that guidelines were not at all influential on their clinical practice

Recommendations for Starting Pap Test Screening

More than 95% of all physicians recommended Pap testing at least every 3 years for the 18-year-old woman who became sexually active 3 years ago (Table 3). Responses for the non–sexually experienced 18-year-old woman were more diverse, with 32% recommending Pap testing annually and 49% recommending no Pap test screening.

Table Jump PlaceholderTable 3.  Responses to Vignettes About Pap Test Screening
Recommendations for Pap Test Screening Frequency

Responses about screening frequency were diverse and were associated with the age of the woman in the vignette as long as the screening and sexual history were the same (Table 3). For example, 42.4% of physicians recommended Pap testing annually for a 25-year-old woman with no new sexual partners in the past 5 years and 3 consecutive negative Pap test results. For a 35-year-old woman with the same sexual and screening history, fewer physicians recommended Pap testing annually. Of note, in the 2 vignettes of a 35-year-old woman with no new sexual partners, which varied only by the number of recent negative Pap test results (3 vs. 1), more than twice as many physicians recommended annual screening for the woman with only 1 negative Pap test result than for the woman with 3 negative Pap test results (78.8% vs. 31.3%).

Recommendations for Stopping Pap Test Screening

For the woman whose cervix was removed for benign reasons, 52.8% of physicians recommended no Pap test (Table 3). For the 66-year-old woman with unresectable NSCLC and for the healthy 71-year-old woman (both with 3 consecutive negative Pap test results), 56.6% and 44.1% of physicians recommended no Pap test, respectively.

Guideline-Consistent Screening Recommendations

Guideline-consistent recommendations varied by specialty across the 4 vignettes included in the composite measure (Figure). More than 95% of physicians had guideline-consistent recommendations for the 18-year-old woman with first sexual intercourse 3 years ago. Closer to half had guideline-consistent recommendations for the other 3 vignettes. The greatest variability across specialty was for the 66-year-old woman with unresectable NSCLC. Overall, 22.3% (CI, 19.9% to 25.0%) of all physicians reported guideline-consistent recommendations for all 4 vignettes included in the composite measure. Guideline-consistent recommendations ranged from 16.4% for OB/GYNs to 21.1% for general or family practice physicians to 27.5% for internists. Because more than 95% of physicians had guideline-consistent recommendations for the only vignette to address underscreening (the 18-year-old woman with first sexual intercourse 3 years ago presenting for her first gynecologic visit), sensitivity analysis excluding this scenario from the composite measure had no appreciable impact on guideline-consistent recommendations. Thus, our guideline-consistent measure represents overuse of screening by primary care physicians.

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Figure.
Guideline-consistent recommendations for Papanicolaou test screening, by physician specialty.

* Guideline-consistent recommendations measured when guidelines are uniform for starting or stopping Papanicolaou testing.

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Controlling for the influence of other physician and practice characteristics in multivariate analysis, specialty was associated with guideline-consistent recommendations (Appendix Table). Compared with OB/GYNs, internists and general or family practice physicians were more likely to have guideline-consistent recommendations (odds ratio, 1.98 [CI, 1.22 to 3.23] and 1.45 [CI, 0.99 to 2.13], respectively; Wald test P < 0.050). Other factors independently associated with guideline-consistent recommendations included board certification, multispecialty practice, and younger physician age (P < 0.050).

Table Jump PlaceholderAppendix Table.  Associations Between Physician and Practice Characteristics and Guideline-Consistent Screening Recommendations

We used a large, nationally representative sample of primary care physicians to identify current Pap test screening practices in the United States during 2006 to 2007. We used clinical vignettes describing women by age and by sexual and screening history to elicit physicians' recommendations for Pap test screening. Fewer than one fourth of physicians reported guideline-consistent recommendations for Pap test screening across vignettes when guidelines were uniform for initiating and stopping screening. Physicians recommended initiating screening in an 18-year-old woman who had not yet had sexual intercourse and continuing screening in patients who had had hysterectomy for benign disease or with unresectable NSCLC. These recommendations reflect overuse of Pap test screening, which is expensive for the health care system (2628) and may result in unnecessary follow-up testing (29) and increased risk for colposcopy-associated illnesses and adverse birth outcomes (30), as well as distress for patients (3134). Quantifying the costs associated with overuse of screening will be an important area for additional research.

We observed overuse in clinical situations in which major guidelines are uniform, and among physicians who describe professional society screening guidelines as being very influential on their clinical practice. Other local guidelines or quality-of-care measures, such as the Healthcare Effectiveness Data and Information Set, may also influence screening recommendations. The Healthcare Effectiveness Data and Information Set measure at the time of the survey was the percentage of women aged 21 to 64 years who had had at least 1 Pap test in the past 3 years (35). Other factors potentially associated with overuse of screening include disagreement with guidelines, confusion due to changes in guidelines over time, financial incentives for more frequent screening, and concerns about malpractice.

To identify English-language studies of physicians' Pap test practices in the United States, we searched MEDLINE through June 2009. Our findings are consistent with other studies (3637) that show that physicians' and other providers' recommendations for Pap test screening are not consistent with guidelines, reflecting initiating screening sooner (3637) and continuing screening in women for whom screening is no longer recommended (3637). As has been reported elsewhere (1719, 21, 23), physician specialty was associated with reported cancer screening practice. Internists, the group with the lowest Pap test volume, were most likely to have guideline-consistent recommendations, followed by general or family practice physicians and OB/GYNs. Although we controlled for the effects of other physician and practice characteristics in multivariate analyses, unmeasured factors, such as training in evidence-based medicine or other primary care practice features, may be related to these specialty differences. We could not directly compare specialty differences with other recent studies of Pap test screening practice conducted in single physician specialties (36, 38) or among other types of providers (for example, nurse or midwife). Compared with a study of OB/GYNs conducted in 2003 (36), the OB/GYNs in our study were more likely to recommend stopping screening for the woman with hysterectomy for benign reasons and more likely to recommend extending Pap test screening intervals for a well-screened, low-risk woman.

In addition to differences in performance by physician specialty, we also found that younger physicians; those who were board-certified; and those practicing in larger, multispecialty settings were more likely to conform to Pap test guidelines. These findings are consistent with other studies showing higher levels of preventive care delivery among younger and more recently trained physicians (39), those who are board-certified (2122), and those in larger practices (21).

Our findings are also consistent with overuse of Pap testing reported by women, particularly among those who had hysterectomy (67) and are at extremely low risk for cervical cancer. Patients may also play a role in overuse of cancer screening. Women in the United States have been reported to be resistant to less-than-annual Pap test screening, even if recommended by their physician (40) or if they no longer have a cervix (40), although more recent studies suggest that women are receptive to being screened less often after a negative HPV test result (41).

Many effective physician-targeted interventions have been developed to increase cancer screening (4243). Although we observed little underuse of Pap testing (<3%) for an 18-year-old woman with first sexual intercourse 3 years ago, improving screening in this group still remains an important cancer control objective, because most cervical cancer cases in the United States occur in women who have never or rarely been screened (5). Strategies to improve guideline-consistent screening will need to consider the possibility of over- and underuse of Pap testing as well as more comprehensive models of patient-, physician-, and system-level influences on screening. Multilevel theoretical models of factors that influence and explain overuse of health services have been applied to the overuse of antibiotics (44) and diagnostic tests (4546). Currently, Medicare does not pay for annual Pap tests in well-screened, low-risk women, and the National Breast and Cervical Cancer Early Detection Program supports extending intervals for women with 3 consecutive negative Pap test results (47). Incorporation of reimbursement policies may be an important component of targeted interventions to improve guideline-consistent use of Pap test screening.

Despite the strengths of using a large national, population-based sample of primary care physicians with a high survey response rate, our study had several limitations. We used standardized clinical vignettes to elicit physician Pap test screening practices, which may not reflect the diversity of women seen in clinical practice. These vignettes contained key components of screening guidelines, including age, screening history, sexual history, and comorbid conditions, but not information about possible sexual contact without intercourse, HPV status, or HPV cotesting that could influence recommendations about Pap testing. Evaluating the role of HPV cotesting will be an important area for additional research.

Vignettes have been used in other settings to elicit information about physician practices (36), and our vignettes were cognitively tested in physicians before fielding the survey. We did not validate the individual vignettes or the composite measure, however. By combining 4 vignettes into a single composite measure, the probability of having guideline-consistent recommendations was lower than with any single vignette. However, because physicians see a variety of patients, this composite measure may more accurately reflect the diversity of clinical practice. Finally, our estimates of screening practices are based on physician self-reports that were not validated through medical records review. Earlier studies have shown that physician self-report overstates practices they believe to be recommended (for example, patient receipt of cancer screening [48]), although more recent studies (49) suggest that physician self-report of practice is reliable. Any idealized reports of practice would imply that guideline-consistent screening recommendations are lower than reported here.

In summary, we observed that primary care physicians' recommendations for Pap test screening are generally not consistent with major guidelines, and reflect overuse of screening. Recommendations varied by physician and practice characteristics. Although guidelines were reportedly influential, they are only 1 factor influencing decisions to recommend screening. Development and dissemination of effective interventions that focus on potentially modifiable physician- and practice-level factors will be important for facilitating cervical cancer screening practices that are consistent with the most recent scientific evidence.

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ACOG Committee on Practice Bulletins.  ACOG Practice Bulletin: clinical management guidelines for obstetrician-gynecologists. Number 45, August 2003. Cervical cytology screening (replaces committee opinion 152, March 1995). Obstet Gynecol. 2003; 102:417-27. PubMed
 
National Cancer Institute, Centers for Disease Control and Prevention, and Agency for Healthcare Research and Quality.  National Survey of Primary Care Physicians' Recommendations & Practice for Breast, Cervical, Colorectal, & Lung Cancer Screening. Accessed athealthservices.cancer.gov/surveys/screening_rp/on 10 September 2009.
 
National Cancer Institute, Centers for Disease Control and Prevention, and Agency for Healthcare Research and Quality.  National Survey of Primary Care Physicians' Cancer Screening Recommendations and Practices: Breast and Cervical Cancer Screening Questionnaire. Accessed athealthservices.cancer.gov/surveys/screening_rp/screening_rp_breast_cervical_inst.pdfon 9 September 2009.
 
Klabunde CN, Frame PS, Meadow A, Jones E, Nadel M, Vernon SW.  A national survey of primary care physicians' colorectal cancer screening recommendations and practices. Prev Med. 2003; 36:352-62. PubMed
 
Yabroff KR, Klabunde CN, Myers R, Brown ML.  Physician recommendations for follow-up of positive fecal occult blood tests. Med Care Res Rev. 2005; 62:79-110. PubMed
 
Hawley ST, Levin B, Vernon SW.  Colorectal cancer screening by primary care physicians in two medical care organizations. Cancer Detect Prev. 2001; 25:309-18. PubMed
 
Schwartz JS, Lewis CE, Clancy C, Kinosian MS, Radany MH, Koplan JP.  Internists' practices in health promotion and disease prevention. A survey. Ann Intern Med. 1991; 114:46-53. PubMed
 
Pham HH, Schrag D, Hargraves JL, Bach PB.  Delivery of preventive services to older adults by primary care physicians. JAMA. 2005; 294:473-81. PubMed
 
Heflin MT, Pollak KI, Kuchibhatla MN, Branch LG, Oddone EZ.  The impact of health status on physicians' intentions to offer cancer screening to older women [Abstract]. J Gerontol. 2006; 61:844-50.
 
Lurie N, Slater J, McGovern P, Ekstrum J, Quam L, Margolis K.  Preventive care for women. Does the sex of the physician matter? N Engl J Med. 1993; 329:478-82. PubMed
 
Research Triangle Institute.  SUDAAN Language Manual: Release 9.0. Research Triangle Park, NC: Research Triangle Institute; 2004.
 
American Association for Public Opinion Research.  Standard Definitions: Final Dispositions of Case Codes and Outcome Rates for Surveys. 5th ed. Lenexa, KS: American Assoc for Public Opinion Research; 2008.
 
Helms LJ, Melnikow J.  Determining costs of health care services for cost-effectiveness analyses: the case of cervical cancer prevention and treatment. Med Care. 1999; 37:652-61. PubMed
 
Ransohoff DF, Lang CA, Kuo HS.  Colonoscopic surveillance after polypectomy: considerations of cost effectiveness. Ann Intern Med. 1991; 114:177-82. PubMed
 
Lafata JE, Simpkins J, Lamerato L, Poisson L, Divine G, Johnson CC.  The economic impact of false-positive cancer screens. Cancer Epidemiol Biomarkers Prev. 2004; 13:2126-32. PubMed
 
Stout NK, Goldhaber-Fiebert JD, Ortendahl JD, Goldie SJ.  Trade-offs in cervical cancer prevention: balancing benefits and risks. Arch Intern Med. 2008; 168:1881-9. PubMed
 
Sadler L, Saftlas A, Wang W, Exeter M, Whittaker J, McCowan L.  Treatment for cervical intraepithelial neoplasia and risk of preterm delivery. JAMA. 2004; 291:2100-6. PubMed
 
Lerman C, Trock B, Rimer BK, Boyce A, Jepson C, Engstrom PF.  Psychological and behavioral implications of abnormal mammograms. Ann Intern Med. 1991; 114:657-61. PubMed
 
Lowe JB, Balanda KP, Del Mar C, Hawes E.  Psychologic distress in women with abnormal findings in mass mammography screening. Cancer. 1999; 85:1114-8. PubMed
 
Lipkus IM, Halabi S, Strigo TS, Rimer BK.  The impact of abnormal mammograms on psychosocial outcomes and subsequent screening. Psychooncology. 2000; 9:402-10. PubMed
 
Aro AR, Pilvikki Absetz S, van Elderen TM, van der Ploeg E, van der Kamp LJ.  False-positive findings in mammography screening induces short-term distress - breast cancer-specific concern prevails longer. Eur J Cancer. 2000; 36:1089-97. PubMed
 
National Committee for Quality Assurance (NCQA).  HEDIS: Health Plan Employer Data and Information Set, 2003. Accessed 15 September 2009 atwww.ncqa.org/tabid/564/Default.aspx.
 
Saint M, Gildengorin G, Sawaya GF.  Current cervical neoplasia screening practices of obstetrician/gynecologists in the US. Am J Obstet Gynecol. 2005; 192:414-21. PubMed
 
Murphy PA, Schwarz EB, Dyer JM.  Cervical cancer screening practices of certified nurse-midwives in the United States. J Midwifery Womens Health. 2008; 53:11-8. PubMed
 
Noller KL, Bettes B, Zinberg S, Schulkin J.  Cervical cytology screening practices among obstetrician-gynecologists. Obstet Gynecol. 2003; 102:259-65. PubMed
 
Schwartz JS, Lewis CE, Clancy C, Kinosian MS, Radany MH, Koplan JP.  Internists' practices in health promotion and disease prevention. A survey. Ann Intern Med. 1991; 114:46-53. PubMed
 
Sirovich BE, Woloshin S, Schwartz LM.  Screening for cervical cancer: will women accept less? Am J Med. 2005; 118:151-8. PubMed
 
Huang AJ, Pérez-Stable EJ, Kim SE, Wong ST, Kaplan CP, Walsh JM. et al.  Preferences for human papillomavirus testing with routine cervical cancer screening in diverse older women. J Gen Intern Med. 2008; 23:1324-9. PubMed
 
Stone EG, Morton SC, Hulscher ME, Maglione MA, Roth EA, Grimshaw JM. et al.  Interventions that increase use of adult immunization and cancer screening services: a meta-analysis. Ann Intern Med. 2002; 136:641-51. PubMed
 
Sabatino SA, Habarta N, Baron RC, Coates RJ, Rimer BK, Kerner J, et al. Task Force on Community Preventive Services.  Interventions to increase recommendation and delivery of screening for breast, cervical, and colorectal cancers by healthcare providers systematic reviews of provider assessment and feedback and provider incentives. Am J Prev Med. 2008; 35:S67-74. PubMed
 
Avorn JL, Barrett JF, Davey PG, McEwen SA, O'Brien TF, Levy SB.  Antibiotic resistance: synthesis of recommendations by expert policy groups. Geneva: World Health Organization; 2001; 1-155.
 
Melanson SE, Szymanski T, Rogers SO, Jarolim P, Frendl G, Rawn JD. et al.  Utilization of arterial blood gas measurements in a large tertiary care hospital. Am J Clin Pathol. 2007; 127:604-9. PubMed
 
Solomon DH, Hashimoto H, Daltroy L, Liang MH.  Techniques to improve physicians' use of diagnostic tests: a new conceptual framework. JAMA. 1998; 280:2020-7. PubMed
 
Cooper CP, Saraiya M, McLean TA, Hannan J, Liesmann JM, Rose SW. et al.  Pap test intervals used by physicians serving low-income women through the National Breast and Cervical Cancer Early Detection Program. J Womens Health. 2005; 14:670-8.
 
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. PubMed
 
Yeazel MW, Lindstrom Bremer KM, Center BA.  A validated tool for gaining insight into clinicians' preventive medicine behaviors and beliefs: the preventive medicine attitudes and activities questionnaire (PMAAQ). Prev Med. 2006; 43:86-91. PubMed
 

Figures

Grahic Jump Location
Appendix Figure.
Identification of primary care physician sample.

AMA = American Medical Association.

Grahic Jump Location
Grahic Jump Location
Figure.
Guideline-consistent recommendations for Papanicolaou test screening, by physician specialty.

* Guideline-consistent recommendations measured when guidelines are uniform for starting or stopping Papanicolaou testing.

Grahic Jump Location

Tables

Table Jump PlaceholderTable 1.  Comparison of Guidelines in 2002 and 2003 for Pap Testing for Cervical Cancer
Table Jump PlaceholderTable 2.  Pap Test Screening Practice and Beliefs, by Physician Specialty
Table Jump PlaceholderTable 3.  Responses to Vignettes About Pap Test Screening
Table Jump PlaceholderAppendix Table.  Associations Between Physician and Practice Characteristics and Guideline-Consistent Screening Recommendations

References

Ries LA, Melbert D, Krapcho M, Stinchcomb DG, Howlader N, Horner MJ. et al.  SEER Cancer Statistic Review, 1975-2005. Bethesda, MD: National Cancer Institute; 2008.
 
Swan J, Breen N, Coates RJ, Rimer BK, Lee NC.  Progress in cancer screening practices in the United States: results from the 2000 National Health Interview Survey. Cancer. 2003; 97:1528-40. PubMed
CrossRef
 
Tiro JA, Saraiya M, Jain N, Liddon N, Cokkinides V, Lai SM. et al.  Human papillomavirus and cervical cancer behavioral surveillance in the US. Cancer. 2008; 113:3013-30. PubMed
 
Tsui J, Saraiya M, Thompson T, Dey T, Richardson L.  Cervical cancer screening among foreign-born women by birthplace and duration in the United States. J Womens Health. 2007; 16:1447-57.
 
Leyden WA, Manos MM, Geiger AM, Weinmann S, Mouchawar J, Bischoff K. et al.  Cervical cancer in women with comprehensive health care access: attributable factors in the screening process. J Natl Cancer Inst. 2005; 97:675-83. PubMed
 
Sirovich BE, Welch HG.  Cervical cancer screening among women without a cervix. JAMA. 2004; 291:2990-3. PubMed
 
Meissner HI, Tiro JA, Haggstrom D, Lu-Yao G, Breen N.  Does patient health and hysterectomy status influence cervical cancer screening in older women? J Gen Intern Med. 2008; 23:1822-8. PubMed
 
Breen N, Wagener DK, Brown ML, Davis WW, Ballard-Barbash R.  Progress in cancer screening over a decade: results of cancer screening from the 1987, 1992, and 1998 National Health Interview Surveys. J Natl Cancer Inst. 2001; 93:1704-13. PubMed
 
Coughlin SS, Thompson TD, Hall HI, Logan P, Uhler RJ.  Breast and cervical carcinoma screening practices among women in rural and nonrural areas of the United States, 1998-1999. Cancer. 2002; 94:2801-12. PubMed
 
Mamon JA, Shediac MC, Crosby CB, Sanders B, Matanoski GM, Celentano DD.  Inner-city women at risk for cervical cancer: behavioral and utilization factors related to inadequate screening. Prev Med. 1990; 19:363-76. PubMed
 
Coughlin SS, Breslau ES, Thompson T, Benard VB.  Physician recommendation for Papanicolaou testing among U.S. women, 2000. Cancer Epidemiol Biomarkers Prev. 2005; 14:1143-8. PubMed
 
U.S. Preventive Services Task Force.  Screening for cervical cancer: recommendations and rationale. Am J Nurs. 2003; 103. PubMed
 
Saslow D, Runowicz CD, Solomon D, Moscicki AB, Smith RA, Eyre HJ, et al. American Cancer Society.  American Cancer Society guideline for the early detection of cervical neoplasia and cancer. CA Cancer J Clin. 2002; 52:342-62. PubMed
 
ACOG Committee on Practice Bulletins.  ACOG Practice Bulletin: clinical management guidelines for obstetrician-gynecologists. Number 45, August 2003. Cervical cytology screening (replaces committee opinion 152, March 1995). Obstet Gynecol. 2003; 102:417-27. PubMed
 
National Cancer Institute, Centers for Disease Control and Prevention, and Agency for Healthcare Research and Quality.  National Survey of Primary Care Physicians' Recommendations & Practice for Breast, Cervical, Colorectal, & Lung Cancer Screening. Accessed athealthservices.cancer.gov/surveys/screening_rp/on 10 September 2009.
 
National Cancer Institute, Centers for Disease Control and Prevention, and Agency for Healthcare Research and Quality.  National Survey of Primary Care Physicians' Cancer Screening Recommendations and Practices: Breast and Cervical Cancer Screening Questionnaire. Accessed athealthservices.cancer.gov/surveys/screening_rp/screening_rp_breast_cervical_inst.pdfon 9 September 2009.
 
Klabunde CN, Frame PS, Meadow A, Jones E, Nadel M, Vernon SW.  A national survey of primary care physicians' colorectal cancer screening recommendations and practices. Prev Med. 2003; 36:352-62. PubMed
 
Yabroff KR, Klabunde CN, Myers R, Brown ML.  Physician recommendations for follow-up of positive fecal occult blood tests. Med Care Res Rev. 2005; 62:79-110. PubMed
 
Hawley ST, Levin B, Vernon SW.  Colorectal cancer screening by primary care physicians in two medical care organizations. Cancer Detect Prev. 2001; 25:309-18. PubMed
 
Schwartz JS, Lewis CE, Clancy C, Kinosian MS, Radany MH, Koplan JP.  Internists' practices in health promotion and disease prevention. A survey. Ann Intern Med. 1991; 114:46-53. PubMed
 
Pham HH, Schrag D, Hargraves JL, Bach PB.  Delivery of preventive services to older adults by primary care physicians. JAMA. 2005; 294:473-81. PubMed
 
Heflin MT, Pollak KI, Kuchibhatla MN, Branch LG, Oddone EZ.  The impact of health status on physicians' intentions to offer cancer screening to older women [Abstract]. J Gerontol. 2006; 61:844-50.
 
Lurie N, Slater J, McGovern P, Ekstrum J, Quam L, Margolis K.  Preventive care for women. Does the sex of the physician matter? N Engl J Med. 1993; 329:478-82. PubMed
 
Research Triangle Institute.  SUDAAN Language Manual: Release 9.0. Research Triangle Park, NC: Research Triangle Institute; 2004.
 
American Association for Public Opinion Research.  Standard Definitions: Final Dispositions of Case Codes and Outcome Rates for Surveys. 5th ed. Lenexa, KS: American Assoc for Public Opinion Research; 2008.
 
Helms LJ, Melnikow J.  Determining costs of health care services for cost-effectiveness analyses: the case of cervical cancer prevention and treatment. Med Care. 1999; 37:652-61. PubMed
 
Ransohoff DF, Lang CA, Kuo HS.  Colonoscopic surveillance after polypectomy: considerations of cost effectiveness. Ann Intern Med. 1991; 114:177-82. PubMed
 
Lafata JE, Simpkins J, Lamerato L, Poisson L, Divine G, Johnson CC.  The economic impact of false-positive cancer screens. Cancer Epidemiol Biomarkers Prev. 2004; 13:2126-32. PubMed
 
Stout NK, Goldhaber-Fiebert JD, Ortendahl JD, Goldie SJ.  Trade-offs in cervical cancer prevention: balancing benefits and risks. Arch Intern Med. 2008; 168:1881-9. PubMed
 
Sadler L, Saftlas A, Wang W, Exeter M, Whittaker J, McCowan L.  Treatment for cervical intraepithelial neoplasia and risk of preterm delivery. JAMA. 2004; 291:2100-6. PubMed
 
Lerman C, Trock B, Rimer BK, Boyce A, Jepson C, Engstrom PF.  Psychological and behavioral implications of abnormal mammograms. Ann Intern Med. 1991; 114:657-61. PubMed
 
Lowe JB, Balanda KP, Del Mar C, Hawes E.  Psychologic distress in women with abnormal findings in mass mammography screening. Cancer. 1999; 85:1114-8. PubMed
 
Lipkus IM, Halabi S, Strigo TS, Rimer BK.  The impact of abnormal mammograms on psychosocial outcomes and subsequent screening. Psychooncology. 2000; 9:402-10. PubMed
 
Aro AR, Pilvikki Absetz S, van Elderen TM, van der Ploeg E, van der Kamp LJ.  False-positive findings in mammography screening induces short-term distress - breast cancer-specific concern prevails longer. Eur J Cancer. 2000; 36:1089-97. PubMed
 
National Committee for Quality Assurance (NCQA).  HEDIS: Health Plan Employer Data and Information Set, 2003. Accessed 15 September 2009 atwww.ncqa.org/tabid/564/Default.aspx.
 
Saint M, Gildengorin G, Sawaya GF.  Current cervical neoplasia screening practices of obstetrician/gynecologists in the US. Am J Obstet Gynecol. 2005; 192:414-21. PubMed
 
Murphy PA, Schwarz EB, Dyer JM.  Cervical cancer screening practices of certified nurse-midwives in the United States. J Midwifery Womens Health. 2008; 53:11-8. PubMed
 
Noller KL, Bettes B, Zinberg S, Schulkin J.  Cervical cytology screening practices among obstetrician-gynecologists. Obstet Gynecol. 2003; 102:259-65. PubMed
 
Schwartz JS, Lewis CE, Clancy C, Kinosian MS, Radany MH, Koplan JP.  Internists' practices in health promotion and disease prevention. A survey. Ann Intern Med. 1991; 114:46-53. PubMed
 
Sirovich BE, Woloshin S, Schwartz LM.  Screening for cervical cancer: will women accept less? Am J Med. 2005; 118:151-8. PubMed
 
Huang AJ, Pérez-Stable EJ, Kim SE, Wong ST, Kaplan CP, Walsh JM. et al.  Preferences for human papillomavirus testing with routine cervical cancer screening in diverse older women. J Gen Intern Med. 2008; 23:1324-9. PubMed
 
Stone EG, Morton SC, Hulscher ME, Maglione MA, Roth EA, Grimshaw JM. et al.  Interventions that increase use of adult immunization and cancer screening services: a meta-analysis. Ann Intern Med. 2002; 136:641-51. PubMed
 
Sabatino SA, Habarta N, Baron RC, Coates RJ, Rimer BK, Kerner J, et al. Task Force on Community Preventive Services.  Interventions to increase recommendation and delivery of screening for breast, cervical, and colorectal cancers by healthcare providers systematic reviews of provider assessment and feedback and provider incentives. Am J Prev Med. 2008; 35:S67-74. PubMed
 
Avorn JL, Barrett JF, Davey PG, McEwen SA, O'Brien TF, Levy SB.  Antibiotic resistance: synthesis of recommendations by expert policy groups. Geneva: World Health Organization; 2001; 1-155.
 
Melanson SE, Szymanski T, Rogers SO, Jarolim P, Frendl G, Rawn JD. et al.  Utilization of arterial blood gas measurements in a large tertiary care hospital. Am J Clin Pathol. 2007; 127:604-9. PubMed
 
Solomon DH, Hashimoto H, Daltroy L, Liang MH.  Techniques to improve physicians' use of diagnostic tests: a new conceptual framework. JAMA. 1998; 280:2020-7. PubMed
 
Cooper CP, Saraiya M, McLean TA, Hannan J, Liesmann JM, Rose SW. et al.  Pap test intervals used by physicians serving low-income women through the National Breast and Cervical Cancer Early Detection Program. J Womens Health. 2005; 14:670-8.
 
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. PubMed
 
Yeazel MW, Lindstrom Bremer KM, Center BA.  A validated tool for gaining insight into clinicians' preventive medicine behaviors and beliefs: the preventive medicine attitudes and activities questionnaire (PMAAQ). Prev Med. 2006; 43:86-91. PubMed
 

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Summary for Patients

A National Survey of Doctors About Screening for Cervical Cancer

The summary below is from the full report titled “Specialty Differences in Primary Care Physician Reports of Papanicolaou Test Screening Practices: A National Survey, 2006 to 2007.” It is in the 3 November 2009 issue of Annals of Internal Medicine (volume 151, pages 602-611). The authors are K.R. Yabroff, M. Saraiya, H.I. Meissner, D.A. Haggstrom, L. Wideroff, G. Yuan, Z. Berkowitz, W.W. Davis, V.B. Benard, and S.S. Coughlin.

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