10158953440864JAMA Intern MedJAMA Intern MedJAMA internal medicine2168-61062168-611424276745438659610.1001/jamainternmed.2013.12607HHSPA673234ArticleOveruse of Papanicolaou Testing Among Older Women and Among Women Without a CervixKepkaDeannaPhD, MPHBreenNancyPhDKingJessica B.MPHBenardVicki B.PhDSaraiyaMonaMD, MPHCancer Control and Population Sciences, Huntsman Cancer Institute, University of Utah, Salt Lake City (Kepka); College of Nursing, University of Utah, Salt Lake City (Kepka); Health Services and Economics Branch, National Cancer Institute, National Institutes of Health, Rockville, Maryland (Kepka, Breen); Cancer Surveillance Branch, Centers for Disease Control and Prevention, Atlanta, Georgia (King); Epidemiology and Applied Research Branch, Division of Cancer Prevention and Control, National Center for Chronic Disease Prevention and Health Promotion, Centers for Disease Control and Prevention, Atlanta, Georgia (Benard, Saraiya)Corresponding Author: Deanna Kepka, PhD, MPH, Huntsman Cancer Institute, College of Nursing, University of Utah, 2000 Circle of Hope, Room 4144, Salt Lake City, Utah 84112 (deanna.kepka@hci.utah.edu)203201512201406420151742293296

Leading national organizations are increasingly using evidence-based recommendations for Papanicolaou testing. As of 2003, organizations recommended against Papanicolaou testing for women without a cervix following a hysterectomy who do not have a history of high-grade precancerous lesion or cervical cancer and for women older than 65 years with adequate prior screening and who are not at high risk.13 Few studies have investigated overuse of Papanicolaou testing among US women. We aimed to investigate overuse of Papanicolaou testing in relation to cervical cancer screening recommendations.

Methods

A cross-sectional study was conducted using data from the 2010 National Health Interview Survey (NHIS). The NHIS is a nationally representative survey of the civilian non-institutionalized population of the United States that uses a random, stratified, multistage cluster sampling design. Analyses of public use data are considered exempt by the institutional review board (IRB) of the National Cancer Institute; IRB approval and informed consent were obtained in the original study. In 2010, the NHIS included a Cancer Control Supplement, which is the most recently available national data set that includes detailed items on cervical cancer screening and hysterectomy status, including, for the first time, questions to assess date of self-reported hysterectomy. The Cancer Control Supplement, fielded to adults 18 years and older, had a response rate of 60.8%.4 Because women younger than 30 years are less likely to have undergone a hysterectomy, our study sample includes women 30 years and older from NHIS 2010 who responded to questions about Papanicolaou test use and hysterectomy status and reported that their Papanicolaou test was for screening purposes (“part of a routine exam”) (N = 9494).

We examined sociodemographic characteristics for our study sample by hysterectomy status and age. We then investigated timing of most recent Papanicolaou test (within the past year, 1–3 years ago, >3 years ago) by sociodemographic characteristics and by hysterectomy status. National estimates of Papanicolaou testing overuse were calculated using the population weights from the 2010 NHIS. Women who reported a history of cervical cancer, an abnormal Papanicolaou test result within the past 3 years, or whose last Papanicolaou test was not part of a routine test were excluded from the results used to generate the national estimates. SAS-callable SUDAAN, version 9.2, was used in all analyses to account for the stratification and clustering of data within the complex survey design of the NHIS.

Results

Among women reporting a hysterectomy, 34.1%(95% CI, 31.7%–36.6%) reported a Papanicolau test in the past year (Table 1).A total of 64.8%(95% CI, 62.2%–67.3%) of women reporting a hysterectomy also reported a recent Papanicolaou test since their hysterectomy, and among women 65 years and older without a hysterectomy, 58.4% (95% CI, 55.3%–61.4%) reported receipt of a Papanicolaou test in the past 3 years (Table 2), together representing approximately 14 million women.

Discussion

For more than a decade, the US Preventive Services Task Force (USPSTF) has recommended that women discontinue Papanicolaou testing if they have received a total hysterectomy and have no history of cervical cancer or if they are older than 65 years and have ongoing and recent normal Papanicolaou test results.5 Nevertheless, in 2010, nearly two-thirds of women reported a Papanicolaou test since their hysterectomy and approximately one-half of women older than 65 years reported a Papanicolaou test in the past 3 years. With the implementation of the Affordable Care Act, the use of electronic medical records, health care provider reminder systems, decision support, and new strategies to improve quality of care may improve guideline-consistent practices among clinicians.6

Limitations of this study are the use of self-reported data to obtain information on Papanicolaou testing and the lack of detail on type of hysterectomy received and on whether older women were adequately screened prior to stopping use of the test.

Misuse of Papanicolaou testing continues despite USPSTF recommendations, and health care resources could be spent better elsewhere. Targeted efforts are needed to reduce unnecessary testing among older women and women without a cervix in compliance with clinical recommendations for cervical cancer prevention.

Author Contributions: Dr Kepka 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.

Study concept and design: Kepka, Breen, Benard, Saraiya.

Acquisition of data: Breen.

Analysis and interpretation of data: All authors.

Drafting of the manuscript: Kepka, Breen, Benard, Saraiya.

Critical revision of the manuscript for important intellectual content: Kepka, Breen, King, Saraiya.

Statistical analysis: Kepka, Breen, King

Administrative, technical, or material support: Saraiya.

Study supervision: Kepka.

Conflict of Interest Disclosures: None reported.

Disclaimer: The findings and conclusions in this report are those of the authors and do not necessarily represent the official position of the National Institutes of Health or the Centers for Disease Control and Prevention.

Additional Contributions: Helen I. Meissner, PhD, at the Office of Disease Prevention, Tobacco Regulatory Science Program, National Institutes of Health; and Katherine B. Roland, MPH, at the Cancer Surveillance Branch, Centers for Disease Control and Prevention, contributed to the design, data interpretation, and manuscript preparation of this investigation. Drs Meissner and Roland were not compensated for their contributions to this study.

US Preventive Services Task ForceScreening for Cervical Cancer: Recommendations and Rationale2003Rockville, MDAgency for Healthcare Research and QualitySaslowDRunowiczCDSolomonDAmerican Cancer Society. American Cancer Society guideline for the early detection of cervical neoplasia and cancerCA Cancer J Clin200252634236212469763ACOG Committee on Practice BulletinsACOG Practice Bulletin: clinical management guidelines for obstetrician-gynecologists. number 45, August 2003. cervical cytology screening (replaces committee opinion 152, March 1995)Obstet Gynecol2003102241742712907124RolandKBBenardVBSomanABreenNKepkaDSaraiyaMCervical cancer screening among young adult women in the United StatesCancer Epidemiol Biomarkers Prev2013224580588.23355601US Preventive Services Task ForceGuide to Clinical Preventive Services19962nd ed.Baltimore, MDLippincott Williams & WilkinsUS Department of Health and Human ServicesKey Features of the Affordable Care Act by YearAccessed October 18, 2013http://www.hhs.gov/healthcare/facts/timeline/timeline-text.html

Characteristics of Women by Hysterectomy Status and by Age, National Health Interview Survey (NHIS) (2010)a

CharacteristicWomen 30 Years and OlderWomen 65 Yearsand Older, No.(% [95% CI])(n = 2581)
Reporting NoHysterectomy, No.(% [95% CI])(n = 7216)Reporting Hysterectomy(n = 2278)
No. (% [95% CI])Mean, y
Age atHysterectomyTime SinceHysterectomy
All women41.320.2
Age, y
  30–442748 (38.1 [36.8–39.5])156 (7.3 [6.1–8.7])33.95.9
  45–642960 (43.7 [42.3–45.0])1049 (49.6 [47.2–52.1])40.015.7
  ≥651508 (18.2 [17.2–19.3])1073 (43.1 [40.7–45.5])44.229.9
Race/ethnicity
  Non-Hispanic white4214 (70.3 [69.0–71.6])1502 (75.1 [73.1–77.1])41.422.01848 (81.0 [79.2–82.7])
  Non-Hispanic black1149 (11.2 [10.3–12.1])439 (13.6 [12.1–15.4])39.719.0369 (8.9 [7.7–10.2])
  Hispanic or Latino1346 (12.5 [11.6–13.4])258 (8.0 [6.9–9.4])41.815.5255 (6.6 [5.7–7.7])
  Other507 (6.0 [5.3–6.7])79 (3.2 [2.5–4.1])42.717.1109 (3.5 [2.8–4.4])
Education
  Less than high school1122 (12.2 [11.3–13.2])430 (15.4 [13.7–17.2])40.724.9611 (20.0 [18.3–21.9])
  High school graduate or GED1785 (24.5 [23.2–25.7])753 (35.4 [33.1–37.8])41.021.2853 (33.8 [31.8–35.9])
  Some college2105 (29.8 [28.6–31.1])703 (31.1 [29.0–33.3])40.420.2663 (27.1 [25.2–29.1])
  College graduate2188 (33.5 [31.9–35.1])384 (18.2 [16.2–20.3])43.618.1440 (19.0 [17.1–21.1])
  Missing16814
Proportion of poverty level, %
  <2003230 (36.8 [35.3–38.4])1126 (41.8 [39.5–44.2])40.523.11418 (47.9 [45.5–50.3])
  200 to <4001465 (21.4 [20.3–22.6])494 (22.8 [21.0–24.8])41.721.5551 (23.5 [21.4–25.7])
  ≥4002519 (41.8 [40.1–43.4])658 (35.3 [32.9–37.8])41.918.1612 (28.6 [26.3–31.1])
  Missing2
Health care coverageb
  Private only2003 (30.2 [28.7–31.7])434 (22.2 [20.1–24.4])39.814.2c
  Public only1491 (16.3 [15.3–17.4])695 (25.5 [23.5–27.5])41.526.31209 (42.9 [40.5–45.4])
  Public and private2639 (40.0 [38.5–41.6])955 (44.6 [42.1–47.0])42.622.21315 (54.9 [52.4–57.4])
  None1069 (13.4 [12.4–14.5])189 (7.8 [6.6–9.2])37.115.8c
  Missing14557
Has a usual source of health care
  Yes6428 (90.2 [89.4–91.0])2161 (95.2 [94.0–96.1])41.521.02504 (97.5 [96.8–98.1])
  No788 (9.8 [9.0–10.6])116 (4.8 [3.9–6.0])37.519.076 (2.5 [1.9–3.2])
  Missing011
Ever heard of HPV
  Yes4141 (75.4 [74.0–76.8])830 (73.1 [70.1–75.9])39.513.9d
  No1554 (24.6 [23.2–26.0])371 (26.9 [24.1–29.9])38.316.1d
  Missing15211077
Time since most recent Papanicolaou test, ye
  <13790 (54.4 [52.9–55.9])724 (34.1 [31.7–36.6])41.616.0659 (27.2 [24.9–29.6])
  1–31880 (26.3 [25.1–27.5])494 (21.7 [19.8–23.7])40.219.7582 (23.2 [21.2–25.3])
  >31490 (19.3 [18.2–20.4])1036 (44.2 [41.8–46.5])41.625.21291 (49.6 [47.2–52.1])
  Missing562449
No. of Papanicolaou tests in past 6 y
  0782 (9.9 [9.1–10.9])718 (31.1 [28.8–33.5])41.126.8907 (34.7 [32.4–37.2])
  1681 (9.2 [8.4–10.0])264 (11.5 [10.0–13.2])41.721.0326 (12.8 [11.4–14.4])
  2660 (9.0 [8.3–9.9])210 (9.0 [7.7–10.5])40.422.4250 (10.1 [8.7–11.6])
  3808 (11.4 [10.6–12.2])203 (9.9 [8.4–11.7])40.219.5255 (11.0 [9.5–12.7])
  4513 (6.7 [6.1–7.4])128 (5.6 [4.6–6.7])41.816.7129 (4.7 [3.8–5.7])
  5535 (8.2 [7.4–9.2])102 (4.8 [3.8–6.1])41.919.2122 (5.3 [4.2–6.6])
  63032 (44.4 [42.9–45.9])593 (26.9 [24.9–29.1])41.615.9504 (21.2 [19.2–23.2])
  ≥793 (1.1 [0.0–1.4])cccc
  Missing1126088

Abbreviations: GED, General Education Development; HPV, human papillomavirus.

Includes all women 30 years and older, excluding women who report history of cervical cancer or an abnormal Papanicolaou test result in the past 3 years and women whose last Papanicolaou test was not a routine test (meaning that women who never had a Papanicolaou test are excluded). Mean age at hysterectomy and mean time since hysterectomy are missing for 105 of the 2278 women who report a hysterectomy. Percentages are weighted estimates. Missing responses are not included in the denominator. All analyses account for the stratification and clustering of data within the complex survey design of the NHIS.

Private insurance includes military insurance; public insurance includes Medicaid, Medicare, State Children’s Health Insurance Program (SCHIP), Indian Health Service (IHS), and other public and other government insurance types; single service plan is considered underinsured and is included with uninsured.

Suppressed because of count less than 50 and/or relative standard error greater than 0.30.

Women 65 years and older were not asked whether they had ever heard of HPV.

Excludes women who did not have a Papanicolaou test in the past 3 years.

Receipt of a Papanicolaou Test Among Women 30 Years and Older by Hysterectomy Status and Sociodemographic Characteristics, National Health Interview Survey (NHIS) (2010)a

CharacteristicWomen Who Received a Papanicolaou Test Within the Past 3 Years, No. (% [95% CI])
Reporting HysterectomybReporting No Hysterectomy
Total1705 (64.8 [62.2–67.3])7160 (80.7 [79.6–81.8])
Age, y
  30–4497 (87.8 [79.5–93.1])2738 (87.8 [86.1–89.3])
  45–64836 (73.3 [69.8–76.6])2947 (83.8 [82.0–85.4])
  ≥65772 (50.8 [46.5–55.0])1475 (58.4 [55.3–61.4])
Race/ethnicity
  Non-Hispanic white1126 (61.5 [58.4–64.4])4179 (79.7 [78.2–81.1])
  Non-Hispanic black337 (76.3 [70.3–81.3])1140 (82.2 [79.6–84.5])
  Hispanic or Latino190 (74.2 [66.9–80.3])1337 (83.0 [80.3–85.4])
  Other52 (70.9 [54.4–83.3])504 (85.4 [81.5–88.6])
Education
  Less than high school318 (56.2 [49.4–62.7])1107 (66.7 [63.0–70.2])
  High school graduate or GED570 (64.1 [59.3–68.6])1764 (73.0 [70.7–75.3])
  Some college523 (69.6 [65.0–73.8])2090 (83.0 [81.0–84.8])
  College graduate or greater291 (66.1 [59.3–72.2])2184 (89.3 [87.8–90.7])
  Missing315
Proportion of poverty level, %
  <200832 (57.6 [53.2–61.8])3194 (71.5 [69.6–73.3])
  200 to <400368 (61.0 [55.4–66.4])1456 (79.7 [77.3–81.9])
  ≥400505 (75.5 [71.4–79.2])2508 (89.3 [87.8–90.7])
  Missing02
Health care coveragec
  Private only334 (80.3 [74.7–84.9])1996 (88.6 [86.9–90.1])
  Public only514 (52.9 [47.7–58.1])1469 (69.3 [66.2–72.3])
  Public and private710 (63.9 [59.7–67.8])2617 (85.0 [83.4–86.5])
  None144 (62.5 [52.1–71.9])1064 (64.2 [60.8–67.5])
  Missing314
Has a usual source of health care
  Yes1625 (65.4 [62.7–67.9])6379 (82.6 [81.5–83.7])
  No80 (50.8 [36.5–65.0])781 (63.2 [58.8–67.4])

Abbreviation: GED, General Education Development.

All women 30 years and older, excluding women who report history of cervical cancer or an abnormal Papanicolaou test result in the past 3 years and women whose last Papanicolaou test was not a routine test. Percentages are weighted estimates. Missing responses are not included in the denominator. All analyses account for the stratification and clustering of data within the complex survey design of the NHIS.

Among women who reported a hysterectomy more than 3 years ago. Cases in which it could not be determined whether the hysterectomy or the Papanicolaou test came first were excluded.

Private insurance includes military insurance; public insurance includes Medicaid, Medicare, State Children’s Health Insurance Program (SCHIP), Indian Health Service (IHS), other public, and other government insurance types; single service plan is considered underinsured and is included with uninsured.