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ORIGINAL RESEARCH |
From the Division of Cancer Prevention and Control, National Center for Chronic Disease Prevention and Health Promotion, Centers for Disease Control and Prevention; and The Klemm Analysis Group, Atlanta, Georgia.
Address reprint requests to: Mona Saraiya, MD, MPH, Division of Cancer Prevention and Control, Centers for Disease Control and Prevention, Epidemiology and Health Services Research Branch, National Center for Chronic Disease Prevention and Health Promotion, 4770 Buford Highway, NE(K-55), Atlanta, GA 30341; E-mail: yzs2{at}cdc.gov.
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ABSTRACT |
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 ABSTRACT MATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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METHODS: We analyzed two surveys of US women aged 18 years or older, the Behavioral Risk Factor Surveillance System (1992–1997) and the National Health Interview Survey (1993–1994), and one survey of US hospitals (National Hospital Discharge Survey, 1980–1997). We examined the number of women who have had a hysterectomy who had a recent (within 3 years) Papanicolaou smear. We also examined trends in the proportions and rates of hysterectomies by diagnoses and type of procedure that potentially could require a Papanicolaou smear.
RESULTS: From the Behavioral Risk Factor Surveillance System, an estimated 21.2% of US women have had a hysterectomy. Among women who have had a hysterectomy, 78.3% had a recent Papanicolaou smear. Among those reporting no hysterectomy, 82.1% had a recent Papanicolaou smear. Estimates from the National Health Interview Survey were similar. From the National Hospital Discharge Survey, an estimated 6.7% to 15.4% of women with a history of hysterectomy would require a subsequent Papanicolaou smear because they had a diagnosis related to cervical neoplasia or because they had undergone a supracervical hysterectomy. For an estimated 10.6–11.6 million of the 12.5 million women who had a hysterectomy and a recent Papanicolaou smear, that test could be considered unnecessary.
CONCLUSION: Continued Papanicolaou screening of women without an intact uteri may result in excessive use of resources in time and money with minimal impact on decreasing cervical cancer.
The decrease in mortality rates from cervical cancer and in the incidence of this disease over the past 40 years has been largely attributed to detection of early cancer and precancerous lesions using the Papanicolaou smear. There is a growing concern, however, that Papanicolaou smear screening is often used inappropriately for certain populations of women (Noller KL. Screening for vaginal cancer [editorial; comment]. N Engl J Med 1996;335: 1599–600).1–3 The United States Preventive Services Task Force recommends that women who have had hysterectomies in which the cervix was removed should not be screened for cervical cancer with a Papanicolaou smear unless they have a history of cervical cancer or its precursors.4 The ACOG has published several documents that acknowledge that cost-effectiveness of screening for vaginal neoplasia has not been shown, but advocate that cytologic evaluation of the vagina is warranted in women after hysterectomy based on the same list of risk factors for which annual cervical Papanicolaou smears are indicated.5–7 The American Cancer Society maintains that women who have had a hysterectomy should continue with regular Papanicoloau smears.8 To estimate the national prevalence of Papanicolaou smears among women who have had hysterectomies and the proportion of hysterectomies performed in which the woman might require a subsequent Papanicolaou smear, we examined two national databases for self-reported prevalence of Papanicolaou smear screening and history of hysterectomy and a third national database to determine trends over time in hysterectomy procedures and diagnoses.
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MATERIALS AND METHODS |
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ABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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To externally validate the Behavioral Risk Factor Surveillance System estimates, we compared them with estimates from the National Health Interview Survey for 1993 to 1994. The National Health Interview Survey uses a multistage probability sampling design to obtain health and demographic data through household, in-person interviews with a sample of the civilian, noninstitutionalized US population aged 18 years or older. We chose the years 1993 and 1994 because the National Health Interview Survey questions about Papanicolaou smear screening and hysterectomy were similarly worded during those 2 years and were comparable to the Behavioral Risk Factor Surveillance System. Women were asked: "About how long has it been since you had a Pap smear test? Was it within the past year, between 1 to 3 years ago, or over 3 years ago?" Women were also asked: "Have you had a hysterectomy?" We analyzed data on 23,123 women aged 18 years and older.
From both the Behavioral Risk Factor Surveillance System and the National Health Interview Survey, the proportion of women who reported a hysterectomy and age-specific rates of recent (within 3 years) Papanicolaou smear screening were calculated. These proportions were stratified by potential predictors of Papanicolaou smear screening. We included seven demographic variables as potential predictors, four of which were included in both surveys: age (18–39, 40–49, 50–64, 65+ years), race or ethnicity (white, non-Hispanic; black, non-Hispanic; other), education (less than high school, high school, or higher), and region (Northeast, Midwest, South, West). Two variables were used only for Behavioral Risk Factor Surveillance System, income (less than $25,000, $25,000 or over, unknown or missing) and insurance status (insured, not insured). Poverty index (at or above poverty index, below poverty index, unknown or missing) was used only for the National Health Interview Survey. The poverty index variable was constructed on family size, number of children under 18 years of age, and family income using the poverty levels from 1992 and 1993 Current Population Survey.10 Using the direct method, estimates of the proportion of women screened for cancer were adjusted to the age distribution of the projected 2000 Census population, as recommended by the National Center for Health Statistics (NCHS).11
We used multivariable logistic regression to determine whether traditional predictors for Papanicolaou smear screening differed by hysterectomy status. Our a priori assumption was that predictors of Papanicolaou smear would differ for the two groups (hysterectomy or no hysterectomy). Unconditional logistic regression with the "change-in-estimate" confounder selection strategy 12 and the Hosmer-Lemeshow goodness-of-fit test13 were used to adjust for the potential demographic variables described above and determine the final model for each dataset.
To take into account the design of the complex, multistage samples, all analyses for Behavioral Risk Factor Surveillance System and the National Health Interview Survey used SUDAAN (professional software for survey data analysis, user documentation for release 7.53, Research Triangle Institute, NC, 1996) to calculate 95% confidence intervals (CI) and to allow for weighting of the estimates. To determine which variables should remain in the final logistic regression model, we used a criterion of P < .05 on the Wald F-test.
A third annual survey, the National Hospital Discharge Survey, uses a national probability sample of inpatient admissions to noninstitutional general and short-stay hospitals; its methodology has been detailed previously.14,15 We used data for 1980–1997 to estimate the proportion of all cases of hysterectomies in which the woman might require subsequent Papanicolaou smears. A 1988 redesign of the National Health Discharge Survey resulted in a new sample of hospitals, and several revisions in data collection and estimation procedures; these changes resulted in lower estimated rates of hysterectomies, and thus, trends for the entire period could not be examined. Accordingly, 1980–1987 and 1988–1997 were evaluated separately.
For hysterectomy, we included any procedures coded as 68.3–68.8 (International Classification of Diseases, 9th Revision, Clinical Modification, procedure code).16 These included total abdominal, subtotal abdominal (or supracervical), vaginal, radical abdominal, radical vaginal, and pelvic exenteration. To determine the indications for hysterectomy, a maximum of seven diagnostic and four procedural codes collected from the hospital discharge form were reviewed. The primary diagnosis was assigned by using the following hierarchy: cervical cancer, other pelvic cancers, carcinoma in situ (CIS) of the cervix, cervical intraepithelial neoplasia (CIN) of the cervix, and all other benign conditions. For example, if cervical cancer was listed as one of the diagnoses, we always made it the primary diagnosis for hysterectomy. For analyses, we divided diagnoses into three major categories: related to cervical cancer (CIS, CIN, cervical cancer), other malignant conditions not related to cervical cancer, and other benign conditions (endometriosis, uterine leiomyoma, uterine prolapse, etc). We divided procedures into four categories: supracervical hysterectomy, total abdominal hysterectomy, total vaginal hysterectomy, and radical hysterectomy, which included pelvic exenteration.
Linear trends in hysterectomy procedures and diagnoses from the National Health Discharge Survey were analyzed by using the weighted least squares regression method, with the inverse of the variances of each annual estimate as the weights.17 The regression used one data point per year, with the year value as the independent variable and the point estimate of the rate as the dependent variable, and the variance of the rate estimate was used to derive the weight. The population estimates of the female civilian residents of the United States used to compute rates were obtained from the United States Bureau of the Census (personal communication, M. Owings, CDC NCHS, 1999). Standard errors for hysterectomy rates were estimated by using the NCHS generalized variance surveys for 1980–1987 and SUDAAN software for complex sample surveys for 1988–1997. For linear tests of trend for the rates, a P value of <.05 was considered significant. The linear test of trend is presented on log scale to accommodate the range of conditions and diagnoses. A separate linear test of trend was conducted for each of the two periods.
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RESULTS |
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). For the Behavioral Risk Factor Surveillance System, the estimate was 21.2% (95% CI 21.0, 21.4) and for the National Health Interview Survey, it was 20.3% (95% CI 19.7, 20.9). We found that the proportion of women who had a hysterectomy increases with age with almost 40.0% of women aged 50 years and older reporting having had the procedure. Black women had a higher proportion of hysterectomy in all age groups except the youngest. Women in the South were more likely than other women to have had a hysterectomy, but regional differences disappeared with stratification by race (results not shown).
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and Table 3). In the Behavioral Risk Factor Surveillance System, 78.3% (95% CI 77.30, 79.3) of women who had hysterectomies had a Papanicolaou smear in the previous 3 years, compared with 82.1% (95% CI 81.8, 82.3) of women who did not have a hysterectomy (Table 2). Regardless of hysterectomy, women with no insurance or lower income were less likely to have had a recent Papanicolaou smear than insured women or those with a higher income, respectively (P < .001). The estimates from the Behavioral Risk Factor Surveillance System are slightly higher than those from the National Health Interview Survey (Table 3), but the characteristics associated with a recent Papanicolaou smear were similar to those found in the National Health Interview Survey.
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Using logistic regression and controlling simultaneously for multiple variables, we again found that predictors of a recent Papanicolaou smear did not vary by hysterectomy status (Table 4). In brief, women who were younger, more educated, insured, had a higher income, and were at or above the poverty index were more likely to have recent screening regardless of hysterectomy status. In addition, black women were more likely to report a recent Papanicolaou smear regardless of hysterectomy status. Women living in certain regions such as the Northeast or Midwest were less likely to report a recent Papanicoloau regardless of hysterectomy.
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). From 1988 to 1997, there was a statistically significant downward trend for hysterectomies with the diagnoses related to cervical neoplasia, from 7.9 (95% CI 6.3, 9.5) in 1988 to 4.0 (95% CI 3.3, 4.7) per 10,000 women in 1997 (Figure 1).
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). Total abdominal (68.9%) and vaginal (29.1%) hysterectomies were the most common; radical hysterectomies represented 1%. The reported annual sample size of supracervical hysterectomies was lower in the first period (range 14–29) than in the second period (range 27–108). No significant trend in supracervical hysterectomy rates was found from 1980 to 1987. However, from 1988 to 1997, the trend toward an increased rate of supracervical hysterectomy was statistically significant (P < .005). In both 1996 and 1997, supracervical hysterectomies accounted for 1.5% of all hysterectomies performed. Adding the proportion range of supracervical hysterectomies and the range of diagnoses related to cervical cancer, our estimate of the percentage of women who have had a hysterectomy who should be getting subsequent Papanicolaou smears is between 6.7% and 15.4%.
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DISCUSSION |
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Our finding that Papanicolaou screening occurs frequently after hysterectomy is consistent with previous analyses. From their retrospective cohort study of a Wisconsin clinic (which validated both hysterectomies and Papanicolaou smears through medical chart review), Eaker et al found that 58% of women who had had hysterectomies for benign causes continued to receive Papanicolaou smear tests, averaging one test every 3 years for women younger than 45 years and one test every 5 years for women 45 years of age and older.3 They concluded this cohort of women received two to three times as many Papanicolaou smears as needed. Kvale et al found slightly lower estimates in their 1993 telephone survey of rural Wisconsin women 40 years and older: 55% of women who had a hysterectomy (for benign disease) more than 3 years ago reported having had a recent Papanicolaou compared with 75% of women who did not have a hysterectomy.22
One reason cited by proponents for the continuation of Papanicolaou smear screening after hysterectomy includes screening for vaginal neoplasia and its precursors.7 However, the low prevalence (1.1%) of vaginal dysplasia or cancer found by Pearce et al among women who had hysterectomy for benign disease and the low positive predictive value for vaginal cancer (0%, 95% CI 0, 33.0%) and vaginal dysplasia (6.3%, 95% CI 3.1%, 18%) they found for the Papanicolaou test in their study suggest that routine vaginal smears should be reserved for women with a history of cancer of the genital tract or cervical CIS.2 Additionally, Fox et al reported that older women who had a hysterectomy had a ten-fold lower risk of a screening test abnormality compared with age-matched women with a uterine cervix.23
Another concern of proponents is the recent increase in number of supracervical hysterectomies. With respect to supracervical hysterectomy, Sills et al reported a significant rise in the supracervical hysterectomy rate from 1991 to 1994 in the rate for this approach per 10,000 women: from 0.16 to 0.41.24 Increased consumer and physician interest in more conservative procedures such as supracervical hysterectomy may be driven by several perceived advantages over total abdominal hysterectomy: it is less invasive, cheaper, less likely to cause bladder dysfunction, and less likely to result in changes in sexual function.25,26 The body of evidence supporting any of these claims for supracervical hysterectomy is sparse,27 however, and is often contradictory.28 In addition, although both the study by Sills et al24 and our own study show a significant increase in the rate of supracervical hysterectomies, such hysterectomies account for a very small proportion (under 1.5%) of all hysterectomies and seem unlikely to become the preferred hysterectomy approach. Eaker et al reported that the screening rate for women who had had a supracervical hysterectomy was the same as those women who had not had a hysterectomy.3 Continued surveillance of hysterectomy procedures and diagnoses that might need continued Papanicolaou smear screening is warranted.
There are several limitations to our study. First, we use self-reported data. Some respondents may have confused pelvic exams with Papanicolaou smears, thereby inflating the percentages. In addition, a recent summary of validation studies reported that women tend to under-report time since their last screen (telescoping),29 but we think this phenomenon would apply equally to women regardless of whether they had undergone a hysterectomy. One study does support a high correlation between self-reports of hysterectomy and hysterectomy status as documented by medical records.30 We also have no information on whether the recent Papanicolaou smear preceded or followed the woman’s hysterectomy. However, the number of hysterectomies that took place in the 3 years prior (1991, 1992, and 1993) adds up to only 1,660,000,14 much lower than the estimated 12.5 million women with a hysterectomy and a recent Papanicolaou test. This argues against the hypothesis that most of these women had the test in preparation for a hysterectomy in the previous 3 years. Therefore, most of the screening is occurring in women who had hysterectomies more than 3 years ago.
Because we could not use the Behavioral Risk Factor Surveillance System and the National Health Interview Survey to examine the type or reason for hysterectomy, we used the National Hospital Discharge Survey to estimate the maximum proportion of hysterectomies for which one could say that a subsequent Papanicolaou smear would be required. Unfortunately, long-term comparisons within the National Hospital Discharge Survey are limited by its redesign in 1988. In addition, indications for hysterectomy could not be independently validated, as pathology reports and medical records were not available for review. Still, the National Hospital Discharge Survey was appropriate to use, as it is the only instrument available for reviewing hysterectomy activity from the 1980s forward.14
Our estimate of the percentage of women who have had a hysterectomy who should be getting subsequent Papanicolaou smears (range 6.7–15.4.%) is dwarfed by our estimate for the percentage of women who have had a hysterectomy and report a recent Papanicolaou smear (range 74.2–78.3%). An estimated 10.6–11.6 million of the 12.5 million women who reported a Papanicolaou test in the past 3 years should not have received one. For this analysis, we assumed that mortality rates for women who have had a hysterectomy whose diagnosis was related to cervical neoplasia were similar to those for women with other diagnoses. We also assumed that all women who had a hysterectomy because of cervical neoplasia-related diagnoses or who had a supracervical hysterectomy had had a recent Papanicolaou smear. Although a more formal analysis using cost-effectiveness and sensitivity techniques is needed, this preliminary calculation points to an area where limiting the inappropriate use of Papanicolaou smears could save substantial monies, anxiety, and unnecessary follow-up of false-positive Papanicolau tests31 for women, insurance providers and purchasers, and the medical and public health communities.
This analysis has implication for many programs including the CDC’s National Breast and Cervical Early Detection Program, which allows low-income and uninsured women access to these cancer screening services in all 50 states, five US territories, and 13 American Indian/Alaska Native programs.32 Although its policy has always been to limit Papanicolaou smear screening to women with an intact cervix or history of cervical neoplasia-related diagnoses, the policy has not been monitored. However, anecdotal reports from funded health agencies that providers were not eliminating women from Papanicolaou screening who had had hysterectomies for benign reasons prompted a policy change. In 1999, all funded programs have been required to have an operational plan to assure that women who have had a total hysterectomy performed for reasons other than cervical neoplasia are not being provided program-funded Papanicolaou smears.
Despite recommendations to screen women with an intact cervix or women with a history of cervical cancer or its precursors, the practice of Papanicolaou screening among women who have had a hysterectomy appears to be occurring at a high rate. Health care providers should take into account a woman’s hysterectomy status (through documented records or a physical examination) and reason for hysterectomy before screening with a Papanicolaou smear. New and increased efforts should target groups who need screening the most: women who have a uterine cervix who are not receiving regular Papanicolaou smear screening.33
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Footnotes |
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Received January 2, 2001. Received in revised form April 16, 2001. Accepted April 19, 2001.
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REFERENCES |
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2. Pearce KF, Haefner HK, Sarwar SF, Nolan TE. Cytopathological findings on vaginal Papanicolaou smears after hysterectomy for benign gynecologic disease. N Engl J Med 1996;335:1559–62.
3. Eaker ED, Vierkant RA, Konitzer KA, Remington PL. Cervical cancer screening among women with and without hysterectomies. Obstet Gynecol 1998;91:551–5.[Abstract]
4. United States Preventive Services Task Force. Guide to clinical preventive services. 2nd ed. Baltimore: Williams & Wilkins, 1996.
5. American College of Obstetricians and Gynecologists. Routine cancer screening. ACOG committee opinion no. 247. Washington, DC: American College of Obstetricians and Gynecologists, 2000.
6. American College of Obstetricians and Gynecologists. Cervical cytology: Evaluation and management of abnormalities. ACOG technical bulletin no. 183. Washington, DC: American College of Obstetricians and Gynecologists, 1993.
7. American College of Obstetricians and Gynecologists. ACOG committee opinion no. 152. Washington, DC: American College of Obstetricians and Gynecologists, 1995.
8. Cervical cancer: Prevention and risk factors. Atlanta: American Cancer Society. Available via the Internet at http://www3.cancer.org/cancerinfo. Accessed 2000 Mar 16.
9. Behavioral Risk Factor Surveillance System: 1992–1997 survey data. Atlanta: National Center for Chronic Disease Prevention and Health Promotion, Centers for Disease Control and Prevention, 1999.
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11. Anderson RN, Rosenberg HM. Report on the second workshop on age adjustment. Hyattsville: National Center for Health Statistics, 1998. Vital Health Stat 4(30).
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13. Kleinbaum DG, Kupper LL, Morgenstern H. Epidemiological research: Principles and quantitative methods. New York: Van Nostrand Reinhold, 1982.
14. Lepine LA, Hillis SD, Marchbanks PA, Koonin LM, Morrow B, Kieke BA, Wilcox LS. Hysterectomy surveillance —United States, 1980–1993. MMWR Morb Mortal Wkly Rep 1997;46(SS-4):1–14.[Medline]
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16. United States Health Care Financing Administration. International classification of diseases, 9th revision, clinical modification, 1999.
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18. McCrory D, Matchar DB, Bastian L, Datta S, Hasselbad V, Hickey D, et al. Evaluation of cervical cytology. Rockville: Agency for Health Care Research and Quality, 1999. Evidence report/technology assessment no. 5. AHRQ publication no. 99-E010. Rockville: Agency for Health Care Research and Quality, 1999.
19. Calle EE, Flanders WD, Thun MJ, Martin LM. Demographic predictors of mammography and Pap smear screening in US women. Am J Public Health 1993;83: 53–60.
20. Blackman DK, Bennett EM, Miller DS. Trends in self-reported use of mammograms (1989–1997) and Papanicolaou tests (1991–1997) — Behavioral Risk Factor Surveillance System. MMWR Morb Mortal Wkly Rep 1999;48: 1–23.
21. American College of Obstetricians and Gynecologists. Role of loop electrosurgical excision procedure in the evaluation of abnormal pap test results. ACOG committee opinion no.195. Washington, DC: American College of Obstetricians and Gynecologists, 1997.
22. Kvale KM, Remington PL, Lantz PM. Self-reporting of Papanicolaou smear tests among women after hysterectomy. Wis Med J 1994;93:275–6.[Medline]
23. Fox J, Remington P, Layde P, Klein G. The effect of hysterectomy on the risk of an abnormal screening Papanicolaou test result. Am J Obstet Gynecol 1999;180: 1104–9.[Medline]
24. Sills ES, Saini J, Steiner CA, McGee M, Gretz HF. Abdominal hysterectomy practice patterns in the United States. Int J Gynaecol Obstet 1998;63:277–83.[Medline]
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28. Rhodes JC, Kjerulff KH, Langenberg PW, Guzinski GM. Hysterectomy and sexual functioning. JAMA 1999;282: 1934–41.
29. Newell S, Girgis A, Sanson-Fisher R, Savolainen N. The accuracy of self-reported health behaviors and risk factors relating to cancer and cardiovascular disease in the general population: A critical review. Am J Prev Med 1999;17: 211–29.[Medline]
30. Fowles JB, Fowler E, Craft C, McCoy CE. Comparing claims data and self-reported data with the medical record for Pap smear rates. Eval Health Prof 1997;20:324–42.
31. Bell S, Porter M, Kitchener H, Fraser C, Fisher P, Mann E. Psychological response to cervical screening. Prev Med 1995;24:610–6.[Medline]
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33. Holmquist ND. Revisiting the effect of the Pap test on cervical cancer. Am J Pub Health 2000;90:620–3.
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| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
