Abstract
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.1–3 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.
Table 1.
Characteristics of Women by Hysterectomy Status and by Age, National Health Interview Survey (NHIS) (2010)a
| Characteristic | Women 30 Years and Older | Women 65 Years and Older, No. (% [95% CI]) (n = 2581) |
|||
|---|---|---|---|---|---|
| Reporting No Hysterectomy, No. (% [95% CI]) (n = 7216) |
Reporting Hysterectomy (n = 2278) |
||||
| No. (% [95% CI]) | Mean, y | ||||
| Age at Hysterectomy |
Time Since Hysterectomy |
||||
| All women | … | … | 41.3 | 20.2 | … |
| Age, y | |||||
| 30–44 | 2748 (38.1 [36.8–39.5]) | 156 (7.3 [6.1–8.7]) | 33.9 | 5.9 | … |
| 45–64 | 2960 (43.7 [42.3–45.0]) | 1049 (49.6 [47.2–52.1]) | 40.0 | 15.7 | … |
| ≥65 | 1508 (18.2 [17.2–19.3]) | 1073 (43.1 [40.7–45.5]) | 44.2 | 29.9 | … |
| Race/ethnicity | |||||
| Non-Hispanic white | 4214 (70.3 [69.0–71.6]) | 1502 (75.1 [73.1–77.1]) | 41.4 | 22.0 | 1848 (81.0 [79.2–82.7]) |
| Non-Hispanic black | 1149 (11.2 [10.3–12.1]) | 439 (13.6 [12.1–15.4]) | 39.7 | 19.0 | 369 (8.9 [7.7–10.2]) |
| Hispanic or Latino | 1346 (12.5 [11.6–13.4]) | 258 (8.0 [6.9–9.4]) | 41.8 | 15.5 | 255 (6.6 [5.7–7.7]) |
| Other | 507 (6.0 [5.3–6.7]) | 79 (3.2 [2.5–4.1]) | 42.7 | 17.1 | 109 (3.5 [2.8–4.4]) |
| Education | |||||
| Less than high school | 1122 (12.2 [11.3–13.2]) | 430 (15.4 [13.7–17.2]) | 40.7 | 24.9 | 611 (20.0 [18.3–21.9]) |
| High school graduate or GED | 1785 (24.5 [23.2–25.7]) | 753 (35.4 [33.1–37.8]) | 41.0 | 21.2 | 853 (33.8 [31.8–35.9]) |
| Some college | 2105 (29.8 [28.6–31.1]) | 703 (31.1 [29.0–33.3]) | 40.4 | 20.2 | 663 (27.1 [25.2–29.1]) |
| College graduate | 2188 (33.5 [31.9–35.1]) | 384 (18.2 [16.2–20.3]) | 43.6 | 18.1 | 440 (19.0 [17.1–21.1]) |
| Missing | 16 | 8 | … | … | 14 |
| Proportion of poverty level, % | |||||
| <200 | 3230 (36.8 [35.3–38.4]) | 1126 (41.8 [39.5–44.2]) | 40.5 | 23.1 | 1418 (47.9 [45.5–50.3]) |
| 200 to <400 | 1465 (21.4 [20.3–22.6]) | 494 (22.8 [21.0–24.8]) | 41.7 | 21.5 | 551 (23.5 [21.4–25.7]) |
| ≥400 | 2519 (41.8 [40.1–43.4]) | 658 (35.3 [32.9–37.8]) | 41.9 | 18.1 | 612 (28.6 [26.3–31.1]) |
| Missing | 2 | … | … | … | … |
| Health care coverageb | |||||
| Private only | 2003 (30.2 [28.7–31.7]) | 434 (22.2 [20.1–24.4]) | 39.8 | 14.2 | c |
| Public only | 1491 (16.3 [15.3–17.4]) | 695 (25.5 [23.5–27.5]) | 41.5 | 26.3 | 1209 (42.9 [40.5–45.4]) |
| Public and private | 2639 (40.0 [38.5–41.6]) | 955 (44.6 [42.1–47.0]) | 42.6 | 22.2 | 1315 (54.9 [52.4–57.4]) |
| None | 1069 (13.4 [12.4–14.5]) | 189 (7.8 [6.6–9.2]) | 37.1 | 15.8 | c |
| Missing | 14 | 5 | … | … | 57 |
| Has a usual source of health care | |||||
| Yes | 6428 (90.2 [89.4–91.0]) | 2161 (95.2 [94.0–96.1]) | 41.5 | 21.0 | 2504 (97.5 [96.8–98.1]) |
| No | 788 (9.8 [9.0–10.6]) | 116 (4.8 [3.9–6.0]) | 37.5 | 19.0 | 76 (2.5 [1.9–3.2]) |
| Missing | 0 | 1 | … | … | 1 |
| Ever heard of HPV | |||||
| Yes | 4141 (75.4 [74.0–76.8]) | 830 (73.1 [70.1–75.9]) | 39.5 | 13.9 | d |
| No | 1554 (24.6 [23.2–26.0]) | 371 (26.9 [24.1–29.9]) | 38.3 | 16.1 | d |
| Missing | 1521 | 1077 | … | … | … |
| Time since most recent Papanicolaou test, ye | |||||
| <1 | 3790 (54.4 [52.9–55.9]) | 724 (34.1 [31.7–36.6]) | 41.6 | 16.0 | 659 (27.2 [24.9–29.6]) |
| 1–3 | 1880 (26.3 [25.1–27.5]) | 494 (21.7 [19.8–23.7]) | 40.2 | 19.7 | 582 (23.2 [21.2–25.3]) |
| >3 | 1490 (19.3 [18.2–20.4]) | 1036 (44.2 [41.8–46.5]) | 41.6 | 25.2 | 1291 (49.6 [47.2–52.1]) |
| Missing | 56 | 24 | … | … | 49 |
| No. of Papanicolaou tests in past 6 y | |||||
| 0 | 782 (9.9 [9.1–10.9]) | 718 (31.1 [28.8–33.5]) | 41.1 | 26.8 | 907 (34.7 [32.4–37.2]) |
| 1 | 681 (9.2 [8.4–10.0]) | 264 (11.5 [10.0–13.2]) | 41.7 | 21.0 | 326 (12.8 [11.4–14.4]) |
| 2 | 660 (9.0 [8.3–9.9]) | 210 (9.0 [7.7–10.5]) | 40.4 | 22.4 | 250 (10.1 [8.7–11.6]) |
| 3 | 808 (11.4 [10.6–12.2]) | 203 (9.9 [8.4–11.7]) | 40.2 | 19.5 | 255 (11.0 [9.5–12.7]) |
| 4 | 513 (6.7 [6.1–7.4]) | 128 (5.6 [4.6–6.7]) | 41.8 | 16.7 | 129 (4.7 [3.8–5.7]) |
| 5 | 535 (8.2 [7.4–9.2]) | 102 (4.8 [3.8–6.1]) | 41.9 | 19.2 | 122 (5.3 [4.2–6.6]) |
| 6 | 3032 (44.4 [42.9–45.9]) | 593 (26.9 [24.9–29.1]) | 41.6 | 15.9 | 504 (21.2 [19.2–23.2]) |
| ≥7 | 93 (1.1 [0.0–1.4]) | c | c | c | c |
| Missing | 112 | 60 | … | … | 88 |
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.
Table 2.
Receipt of a Papanicolaou Test Among Women 30 Years and Older by Hysterectomy Status and Sociodemographic Characteristics, National Health Interview Survey (NHIS) (2010)a
| Characteristic | Women Who Received a Papanicolaou Test Within the Past 3 Years, No. (% [95% CI]) | |
|---|---|---|
| Reporting Hysterectomyb | Reporting No Hysterectomy | |
| Total | 1705 (64.8 [62.2–67.3]) | 7160 (80.7 [79.6–81.8]) |
| Age, y | ||
| 30–44 | 97 (87.8 [79.5–93.1]) | 2738 (87.8 [86.1–89.3]) |
| 45–64 | 836 (73.3 [69.8–76.6]) | 2947 (83.8 [82.0–85.4]) |
| ≥65 | 772 (50.8 [46.5–55.0]) | 1475 (58.4 [55.3–61.4]) |
| Race/ethnicity | ||
| Non-Hispanic white | 1126 (61.5 [58.4–64.4]) | 4179 (79.7 [78.2–81.1]) |
| Non-Hispanic black | 337 (76.3 [70.3–81.3]) | 1140 (82.2 [79.6–84.5]) |
| Hispanic or Latino | 190 (74.2 [66.9–80.3]) | 1337 (83.0 [80.3–85.4]) |
| Other | 52 (70.9 [54.4–83.3]) | 504 (85.4 [81.5–88.6]) |
| Education | ||
| Less than high school | 318 (56.2 [49.4–62.7]) | 1107 (66.7 [63.0–70.2]) |
| High school graduate or GED | 570 (64.1 [59.3–68.6]) | 1764 (73.0 [70.7–75.3]) |
| Some college | 523 (69.6 [65.0–73.8]) | 2090 (83.0 [81.0–84.8]) |
| College graduate or greater | 291 (66.1 [59.3–72.2]) | 2184 (89.3 [87.8–90.7]) |
| Missing | 3 | 15 |
| Proportion of poverty level, % | ||
| <200 | 832 (57.6 [53.2–61.8]) | 3194 (71.5 [69.6–73.3]) |
| 200 to <400 | 368 (61.0 [55.4–66.4]) | 1456 (79.7 [77.3–81.9]) |
| ≥400 | 505 (75.5 [71.4–79.2]) | 2508 (89.3 [87.8–90.7]) |
| Missing | 0 | 2 |
| Health care coveragec | ||
| Private only | 334 (80.3 [74.7–84.9]) | 1996 (88.6 [86.9–90.1]) |
| Public only | 514 (52.9 [47.7–58.1]) | 1469 (69.3 [66.2–72.3]) |
| Public and private | 710 (63.9 [59.7–67.8]) | 2617 (85.0 [83.4–86.5]) |
| None | 144 (62.5 [52.1–71.9]) | 1064 (64.2 [60.8–67.5]) |
| Missing | 3 | 14 |
| Has a usual source of health care | ||
| Yes | 1625 (65.4 [62.7–67.9]) | 6379 (82.6 [81.5–83.7]) |
| No | 80 (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.
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.
Footnotes
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.
References
- 1.US Preventive Services Task Force. Screening for Cervical Cancer: Recommendations and Rationale. Rockville, MD: Agency for Healthcare Research and Quality; 2003. [Google Scholar]
- 2.Saslow D, Runowicz CD, Solomon D, et al. American Cancer Society. American Cancer Society guideline for the early detection of cervical neoplasia and cancer. CA Cancer J Clin. 2002;52(6):342–362. doi: 10.3322/canjclin.52.6.342. [DOI] [PubMed] [Google Scholar]
- 3.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(2):417–427. doi: 10.1016/s0029-7844(03)00745-2. [DOI] [PubMed] [Google Scholar]
- 4.Roland KB, Benard VB, Soman A, Breen N, Kepka D, Saraiya M. Cervical cancer screening among young adult women in the United States. Cancer Epidemiol Biomarkers Prev. 2013;22(4):580–588.. doi: 10.1158/1055-9965.EPI-12-1266. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.US Preventive Services Task Force. Guide to Clinical Preventive Services. 2nd ed. Baltimore, MD: Lippincott Williams & Wilkins; 1996. [Google Scholar]
- 6.US Department of Health and Human Services. [Accessed October 18, 2013];Key Features of the Affordable Care Act by Year. http://www.hhs.gov/healthcare/facts/timeline/timeline-text.html.