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Screening Interval and Risk of Invasive Squamous Cell Cervical Cancer

From the Department of Quality and Utilization and Division of Research, Kaiser Permanente Medical Care Program, Oakland, California; Division of Gynecologic Oncology, Kaiser Permanente Medical Care Program, Sacramento, California; Institute for Health and Aging, School of Nursing, and Departments of Obstetrics, Gynecology, & Reproductive Sciences and Epidemiology and Biostatistics, University of California, San Francisco, California.

Address reprint requests to: Marie Grisham Miller, PhD, 2331 Rancho del Lago Road, Martinez, CA 94553; E-mail: mariegmiller{at}saber.net.

	ABSTRACT

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
OBJECTIVE: To compare the risks of developing invasive squamous cell cervical cancer associated with screening intervals of 1, 2, and 3 years after a negative cervical smear.

METHODS: We conducted a matched case-control study of invasive squamous cell cervical cancer patients (n = 482) diagnosed between 1983 and 1995 among long-term members of a large health maintenance organization. Controls were matched for age, length of membership, and race (n = 934). Screening interval was time between the last negative cervical smear and the case diagnosis date. The main outcome measure was the relative odds of invasive disease associated with 1-year, 2-year, and 3-year intervals.

RESULTS: The odds ratio for a 2-year versus a 1-year interval was 1.72 (95% confidence interval 1.12, 2.64, P = .013) and for a 3-year versus a 1-year interval was 2.06 (95% confidence interval 1.21, 3.50, P = .007). The odds ratio for a 3-year versus a 2-year interval was 1.20 (95% confidence interval 0.65, 2.21, P = .561). Controlling for ever having had an abnormal cervical smear or a previous consecutive negative smear did not substantially change these results.

CONCLUSION: In this large health plan, the relative risks of invasive squamous cell cervical cancer were significantly greater for 2-year and 3-year cervical cancer screening intervals compared with a 1-year interval, but not for a 3-year interval compared with a 2-year interval. Our findings need to be placed in the context of the low absolute risks of developing invasive cervical cancer during the first 3 years after a negative cervical smear before making policy recommendation.

Disease screening is effective when the screening test can detect a disease or its precursor before it becomes symptomatic, and when early treatment can improve the patient’s outcome. Papanicolaou smear screening can detect precancerous lesions as well as presymptomatic invasive squamous cell cancer of the uterine cervix, both of which may be treated effectively. Cohort studies have clearly demonstrated this with risk reductions in incidence of and mortality from cervical cancer ranging from 60–90%.^1–7 In the United States between 1973 and 1998, age-adjusted incidence of invasive cervical cancer fell from 14.2 to 7.5 per 100,000 women, and mortality from 5.2 to 2.5 per 100,000 women.⁸

Although the efficacy of Papanicolaou smear screening has been well documented, the optimal interval at which repeat screening should be performed is not clear. Until recently, standard medical practice recommended annual screening, which some organizations still recommend.⁹ Suggestions to increase the interval from 1 to 2 or even 3 years have been adopted by others.¹⁰ Some guidelines recommend two or three annual smears to initiate screening, and if those are negative, intervals up to 3 years between smears may be appropriate.^11–13

The appropriate interval for rescreening depends on the natural history of the disease, especially the duration of the detectable preclinical phase, and the sensitivity of the test. The average detectable preclinical phase of cervical cancer is reported to be relatively long, but its variance is not well described. The International Agency for Research on Cancer noted that although estimates of the average detectable preclinical phase are highly influenced by slow-growing cancers, when proposing to increase the screening interval, it is the left-hand tail of the distribution, the fast-growing cancers, that is of most concern.¹⁴ We performed a case-control study in a large health maintenance organization to compare the relative risks of developing invasive squamous cell cervical cancer associated with intervals of 1, 2, and 3 years after a negative cervical smear.

	MATERIALS AND METHODS

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
The Kaiser Permanente Medical Care Program in Northern California is a large health maintenance organization currently with over 3 million members. Annual cervical smears have been standard practice for 30 years and are offered at no additional fees beyond the nominal visit copay. In addition, screening at prenatal and postpartum visits has been widely practiced. Screening rates among female members are high. An unpublished study from a random survey conducted among adult members in 1996 found that 92% of women aged 20 and above reported they had been screened at least once, and 89% screened at least once within the last 3 years (personal communication, N. P. Gordon, Division of Research, Kaiser Permanente, Oakland, California, April 1997). The Health Plan Employer Data and Information Set studies found that over 78% of female members aged 21–64 continuously enrolled in the Kaiser Permanente Medical Care Program in Northern California from 1994 to 1996 had been screened within 3 years.¹⁵

Potential cases were female members of the Kaiser Permanente Medical Care Program in Northern California initially diagnosed with primary invasive squamous cell cervical cancer between 1983 and 1995. Cases were identified from the Kaiser Permanente Medical Care Program in Northern California Cancer Registry, the Surveillance, Epidemiology, and End Results program of the National Cancer Institute, and the California Cancer Registry. From 1983 to 1987, reporting of cancer cases was only available at Kaiser Permanente Medical Care Program facilities in five counties (San Francisco, San Mateo, Marin, Alameda, and Contra Costa). From 1988 to 1989, reporting of cases was complete within these facilities, except for the Sacramento area. From 1990 to 1995, cases were reported from all these facilities. We excluded women with a prior history of total hysterectomy (ie, no cervical stump remains) or radiation therapy to the pelvis (ie, a history of cervical, vaginal, or uterine cancer). From the remaining potential cases, we selected women with continuous membership in the Kaiser Permanente Medical Care Program in Northern California for at least 30 of the 36 months before diagnosis. Continuous membership assured that complete medical records existed for 3 years before diagnosis.

Our objective, based on statistical power calculations, was to match each case with two controls. The adequacy of sample size depends on both the size of the estimated odds ratios (ORs) for each analysis and the exposure rate of the controls to the targeted screening interval. Based on previous studies, our estimates of possible ranges for ORs for the planned analyses were as follows: test 1 (1-year versus 2-year interval, 0.4–0.9), test 2 (1-year versus 3-year interval, 0.3–0.5), and test 3 (2-year versus 3-year interval, 0.3–0.67). From our laboratory database, we estimated the control exposure rate for each test as follows: test 1 (70%), test 2 (80%), and test 3 (60%). The largest detectable OR for our sample, assuming 80% power, 95% confidence interval (CI), and two controls per case, was calculated. For test 1, the largest detectable OR from our sample was 0.65, for test 2, 0.61, and for test 3, 0.56. These largest detectable ORs were sufficient for us to proceed with the study.

Controls were matched to cases by age, length of membership, and race/ethnicity. The identification of controls was a two-step process. First, computerized membership files identified potential controls on the basis of birth date (within 2 years of matching case), and membership characteristics (members for at least 30–36 months directly before a case diagnosis date, total length of the most recent continuous period of membership, and date of first enrollment). Patients who were members for less than 10 continuous years directly before diagnosis were matched to controls with a similar length of most recent continuous membership (within 6 months) and a similar date of first enrollment (within 3 years). Patients who were members for greater than 10 continuous years before diagnosis were matched with controls who were continuous members for at least 9.5 years before the case diagnosis date regardless of the date of first enrollment. These data were matched to automated hospitalization data to exclude women with a history of total hysterectomy or radiation therapy to the pelvis and to automated mortality data to exclude any women who died before the case diagnosis date. Up to 20 potential controls per case were randomly generated.

In the second step, medical charts of potential controls were consecutively screened by reviewers for a match on the patient’s race/ethnicity (non-Hispanic white, black, Asian, and Hispanic), and for indications of total hysterectomy, invasive cervical cancer, or death before the case diagnosis date. The first two potential controls who met the matching criteria and were not excluded were identified as the matched controls. After several iterations of matching as described above, potential controls were lacking for some black, Asian, and Hispanic subjects. For these women, we relaxed the matching criteria for age (up to 5 years), length of the last continuous membership period (up to 12 months), and date of first enrollment (up to 5 years) to obtain controls.

All data on cervical smear histories were obtained from medical chart review. Two medical record abstractors reviewed the charts of each subject. The first abstractor masked the chart 6 months before the diagnosis date of patients or index date of controls and reviewed the chart for this 6-month period. The diagnosis date for patients was the date of their pathology report. The index date of controls was the diagnosis date of their matched case. Masking was done to avoid differential chart abstraction between cases and controls. The second abstractor, blinded to the status of the subject, abstracted information from the masking date back to the earliest medical record from the Kaiser Permanente Medical Care Program in Northern California or to the age of 18. Both reviewers recorded dates of, reasons for, and results of all cervical smears performed, all diagnostic and therapeutic procedures involving the cervix, and all medical visits within 5 years of the diagnosis or index date. For patients, the first reviewer also recorded the tumor cell type and tumor stage at diagnosis.

Data were abstracted for patients diagnosed from 1988 to 1994 in the first phase of this study.¹⁶ In the second phase, patients diagnosed from 1983 to 1987 and in 1995 and all controls were abstracted. For quality control, a random 5% of charts throughout the course of chart review were reabstracted to assure consistency of the data abstracted. A maximal error rate no greater than 5% was found for key variables (number of cervical smears performed, dates of smears, and smear results). To check for changes in data abstraction between the first and second phases of data collection, 50 patients abstracted in phase one were randomly selected, and their medical charts were blindly reabstracted. Comparison of the second abstraction to the first showed no change in data abstraction as the review progressed.

We classified the result of each smear into one of three categories: "negative" (or "normal"), "abnormal requiring follow-up," and "other." More than one classification system for the cytologic results of cervical smears was used during the study period, necessitating a long list of possible results. A smear was defined as "negative" only if the result was negative regardless of the presence or absence of endocervical cells, or a nondysplastic abnormality not requiring a change in follow-up interval including inflammation, metaplasia, reactive changes, and cervicitis. A smear was defined as "abnormal" if the result was reported as unsatisfactory specimen, atypia, or abnormal not otherwise specified, koilocytic cells, human papillomavirus, condyloma, atypical squamous cells of undetermined significance, class II (mild), "clear & repeat," atypical glandular cells of undetermined significance, atypical squamous and glandular cells of undetermined significance, dysplasia, cervical intraepithelial neoplasia, Papanicolaou class III or class IV, lowgrade squamous intraepithelial lesion, high-grade squamous intraepithelial lesion, squamous carcinoma in situ, probable/suggestive cancer, carcinoma, adenocarcinoma in situ, atypical/dysplastic endocervical cells, endocervical carcinoma, adenocarcinoma not otherwise specified, or invasive carcinoma not otherwise specified. All other smears were classified "other" including smears where the result was missing or unrelated to invasive cervical cancer (eg, atypical/dysplastic endometrial cells, atrophic changes, trichomonas).

Screening interval was length of time between the last negative smear, whether performed for screening or not, and the case diagnosis date. Some patients and controls had no negative smears, and thus had no definable screening interval. Among subjects with at least one negative smear before the diagnosis date, we defined a 1-year interval as 0–18 months, a 2-year interval as 19–30 months, and a 3-year interval as 31–42 months. Longer intervals included 3–5 years (42–66 months), 5–10 years (67–126 months), and more than 10 years (more than 126 months).

The 1-year interval was defined as 18 months rather than 12 months to avoid creating a spurious difference in exposure to negative smears among patients compared with controls.¹⁷ Given the recommendation for annual screening among the Kaiser Permanente Medical Care Program in Northern California members during the study period, women whose cancer was initially diagnosed at a routine "annual" screening would be very unlikely to have had a prior negative smear within the previous 12 months. On the other hand, because the patient’s diagnosis date was unrelated to the matched control’s screening history, the controls were more likely to have had a negative smear within the previous 12 months. Also, in our sample, among women with at least two negative smears, the distribution of the interval between consecutive smears peaked between 12 and 15 months. Defining the first interval as 0–18 months thus allowed us to count all smears intended as part of an annual screening pattern.

We performed conditional logistic regressions for matched case-control data using the PROC PHREG procedure from the SAS statistical package 6 (SAS Institute, Inc., Cary, NC). The dependent variable was a binary variable indicating the status of being a case instead of a control. The reference group was women with a 1-year screening interval. In the unadjusted model, the predictor variables were 2-year, 3-year, and longer intervals as well as the category of never having had a negative cervical smear. We calculated ORs for being a case as opposed to a control associated with different intervals.

Two confounding variables were added to our risk-adjusted model: 1) a history of ever having had an abnormal cervical smear before the last negative cervical smear, and 2) having had at least one previous consecutive negative smear immediately preceding, and within 36 months of, the last negative cervical smear. The first variable was added because it is a potential confounder. A woman with a previous abnormal result may subsequently have more frequent smears as follow-up. Ever having had an abnormal result might thus be associated with both an increased risk of cervical cancer and an increased screening frequency.

The second variable was added to address the well-known problem of false-negative cytology results.^18–20 A recent report on cervical cytology estimated the sensitivity of cervical smears at only 50%.²¹ False-negative results can stem from an inadequate tissue sample, infections contaminating the sample, and human failure in evaluating the smear. We also reran the analysis on the subsample of women with at least one previous consecutive negative cervical smear within 36 months before their last negative smear to address this issue.

	RESULTS

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Between 1983 and 1995, 705 patients were diagnosed with invasive squamous cell cervical cancer in the health plan, and 484 of them were members for at least 30 of 36 months before the diagnosis date. Two of the 484 patients were excluded from the final analysis because we could not find matched controls. The final sample included 482 cases and 934 matched controls. Four hundreds and fifty two cases (94%) had two matched controls, and 30 cases (6%) had one matched control. Cases and controls were very similar demographically as expected because of our matching criteria (Table 1). The mean age of patients was 49.5 years and that of controls was 48.8 years. Both patients (69%) and controls (71%) were predominantly white. Asians (11%), blacks (11%), and Hispanics (8% and 7%) constituted very similar proportions of each sample. Patients and controls were very similar in length of enrollment in the Kaiser Permanente Medical Care Program in Northern California, with 95% of each group’s most recent membership period greater than or equal to 42 months.

	DISCUSSION

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

A number of case-control studies have addressed the issue of the optimal interval between cervical smears.^22–36 Many used as the reference group either "never-screened" women or women whose last negative smear was performed many years ago to estimated the relative protection (the inverse of the relative risk) of a more recent cervical smear. Macgregor et al found relative protections of 6.9 and 3.4 for screening intervals of 2 and 3 years compared with never screened.²² Celentano et al found relative protections of 16.39 for a 1-year interval versus 9.35 for a 2- or 3-year interval.²³ In a study in Toronto, Clarke et al found significant relative protections of 4.7 and 2.6 for intervals of 1 and 2 years compared with never screened, whereas a 3-year interval was not significant.²⁴ Geirsson et al estimated relative protections of 9.7 for a 1-year, 7.0 for a 2-year, and 3.8 for a 3-year interval compared with a more than 10-year interval, thus finding more difference between 1 and 3 years or between 2 and 3 years than between 1 and 2 years.²⁵ Raymond et al found a relative protection of 7.5 for a 1-year interval compared with 2.7 for a 2–3-year interval, even more difference than the present findings.²⁶

Other studies estimated relative risks for shorter intervals using the "never screened" or a similar category for the reference group. La Vecchia et al in a study in Milan found relative risks of 0.10, 0.18, and 0.36 for intervals of less than 3 years, 3–5 years, and more than 5 years, respectively.²⁷ Klassen et al found estimates of relative risk of 0.07 for an interval of less than 1 year, 0.14 for a 2–4-year interval, and 0.38 for a 5-year interval, quite consistent with the present results.²⁸ Berrino et al estimated relative risks of 0.14, 0.16, and 1.16 for intervals of 1, 2, or 3 years compared with never screened.²⁹ Olesen found a relative risk of 0.15 for having had a smear within 3 years, compared with never-screened women.³⁰

More recently, Sato et al found estimates of relative risks of 0.11, 0.33, and 0.65 for screening intervals of 1, 2, and 3–4 years compared with never screened, but only the estimates for 1- and 2-year intervals were statistically significant.³¹ In another analysis from the same sample, Makino et al found estimates of relative risks of 0.09, 0.17, and 0.67 for 1-year, 2-year, and 3-year intervals (all with P = .001).³²

Fewer previous case-control studies used as the reference group women with a 1-year or similar interval. Shy et al found that a 3-year, but not a 2-year, interval significantly increased risk compared with a 1-year interval.³³ Unfortunately, intervals in this study were not calendar based, but calculated based on the number of smears done in a 10-year period. Brinton et al estimated an OR of 2.0 for a cervical smear 3–4 years prior compared with a smear within 2 years.³⁴ Peters et al found that compared with a cervical smear within 2 years, a smear 2–5 years prior had a relative risk of 1.7 (P = .001).³⁵ These estimates of increased relative risk are consistent with our results. In contrast, Herrero et al found no increase in relative risk associated with a screening interval of 2–4 years compared with an interval of 1–2 years. This study had weaknesses in the source of data on cervical smears and the definition of the exposure period, which are discussed below.³⁶

Using case-control methodology to determine the duration of protection from a negative cervical smear is complex. Important elements in a rigorous study design include the following: 1) limit cases to squamous cell cancers, 2) require controls to have intact uteri, 3) obtain data on cervical smears from medical records, not self-report, 4) define the beginning and end of the exposure period based on the detectable preclinical phase, and 5) select a large enough sample to have sufficient power to detect small differences. The current study’s strengths include all of the above.

First, although cervical smears effectively detect squamous cell carcinoma, the evidence regarding adenocarcinoma is less well documented. Studies that included adenocarcinoma along with squamous cell cancer risk diluting the relative efficacy of more recent compared with more distant cervical cancer screening.^{23,26–28,31,32,35} Our study was limited to squamous cell cancers.

Second, because all women with cervical cancer have cervixes by definition, appropriate controls must also have cervixes.³⁷ Women who have undergone hysterectomy are unlikely to have recent cervical smears, and are not at risk for cervical cancer. Such controls may reduce the apparent efficacy of more recent smears compared with more distant smears and obtain biased results.^24,27,35 However, determining hysterectomy status can be quite difficult. Our study excluded both patients and controls who had a history of total hysterectomy or radiation therapy to the pelvis by using the automated hospitalization database and reviewing medical charts.

Third, some studies have used self-reported data on cervical smear history.^{23,27,28,33–36} Self-reported data are problematic.^38–41 Women report more cervical smears than their medical records indicate and report their last smear as more recent than their records show. Patients may remember the number and timing of cervical smears more than controls because of the vividness of their cancer diagnosis. This biased recall may reduce the apparent relative efficacy of more recent smears compared with more distant smears.

Fourth, studies vary in how the beginning of the exposure period is defined. The duration of protection from a cervical smear must begin with a negative smear. Many patients will have had recent positive smears. Including these in the analysis, as some studies have done, will dilute the apparent protection of recent negative smears compared with more distant negative smears.^{23,27,28,33–35} Some studies defined the beginning of the exposure period as the last negative smear done for screening only.^30,32 The distinction between screening and nonscreening tests is immaterial for estimating the duration of protection from a negative cervical smear. This study used the last negative smear as the beginning of the interval whether for screening purposes or not.

The definition of the end point of exposure is also important. Some studies, including the present one, have used the diagnosis date of the case as the end point for both patients and controls. Others have excluded all smears done within a defined period of time (often 6 months or 1 year) before the case diagnosis date.^{24,27,28,32,35,36} These smears were excluded because it was assumed that for patients, these negative smears were either diagnostic, not screening smears, or were false-negatives, and their inclusion would wrongly reduce the apparent relative efficacy of recent smears.

As explained above, we were not concerned with the distinction between screening and nonscreening smears. However, false-negative cytology is a serious problem. The International Agency for Research on Cancer’s meta-analysis found much more consistency of results among the different programs studied when the analysis was restricted to women who had had at least two negative smears, thus reducing the influence of false-negatives. We adjusted for the presence of at least one previous consecutive negative smear within 36 months before the last negative smear in our full sample. In addition, we reran our model on the subsample of women who had had at least two consecutive negative cervical smears before the case diagnosis date, the last two occurring within 36 months of each other. The results were essentially unchanged.

Finally, a study can only demonstrate significant differences when it has adequate statistical power. Power depends upon both the relative frequency of exposure among the controls compared with that for the patients and the estimated size of the effect. The expected differences in relative risk between 1-year, 2-year, and 3-year intervals are not large. Therefore, the sample size required for adequate statistical power is substantial. Two of the earlier studies had only 67 and 85 cases.^22,33 Most of the others had between 100 and 200.^{23–27,29,31} When looking at the number of patients with a smear within 1 year, the sample sizes get even smaller, ranging from 0 to 16. The issue of statistical power is a serious concern for this research question. A large sample was required for this study to be adequately powered. Our sample was one of the largest yet studied.

Our study did not attempt to adjust for risk factors connected to the sexual history of the woman or her partner(s). Such information is difficult to obtain by the physician, and the woman herself may not be fully informed. Thus, it is not useful for rescreening recommendations. Other studies have found that women least likely to be screened are those of low socioeconomic status and less education. The members of the Kaiser Permanente Medical Care Program in Northern California are largely employed persons and their dependents with limited membership of either the very rich or very poor, thus reducing any possible income effect. In addition, lower education and socioeconomic status are positively associated with increased parity. The Kaiser Permanente Medical Care Program in Northern California has for years done opportunistic screening at prenatal and postpartum visits, so those women less likely to come for an annual routine screening smear were still likely to be opportunistically screened. Secondly, membership in the Kaiser Permanente Medical Care Program in Northern California provides access to free or very low-cost screening, removing any economic disincentive for screening. For these reasons, we think confounding related to socioeconomic and educational status is minimized in this study.

In summary, earlier studies found more protection from recent smears than from more distant smears. Increased efficacy with increased frequency of screening is an expected result, and it should be no surprise to find statistically significant evidence of this increased efficacy in a study with sufficient statistical power. However, the design of these earlier studies did not specifically address the policy question of whether, and to what extent, instituting a 2- or 3-year screening interval in a population previously offered annual smears increased the risk of cervical cancer. The important contributions of this study are that our sample size was adequate to decisively demonstrate the increased efficacy of a 1-year interval over a 2-year interval, and that the magnitude of differences between these two short intervals has been more precisely quantified.

These findings need to be placed in the context of the low absolute risks of developing invasive cervical cancer during the first 3 years after a negative smear and the promise of emerging new screening technology. The age-adjusted incidence of invasive cervical cancer among members at the Kaiser Permanente Medical Care Program in Northern California was 6.2 per 100,000 women in 1994. Even a doubling of the relative risk with a 2-year screening interval still leaves the absolute risk small. Nevertheless, this study evaluated the incidence of invasive squamous cell cervical cancer, not mortality from it. When considering a decrease in the frequency of cervical screening, policy makers need to assess not only the increased risk of cervical cancer incidence, but also its impact on morbidity and mortality and the associated direct and indirect costs. Finally, newer screening technologies such as monolayer cytology and human papillomavirus-deoxyribonucleic acid testing will lead to improved detection of important cervical disease.^42–44 Further evaluation of appropriate screening intervals will be required as these new technologies are incorporated into routine screening.

	Footnotes

 
RAH is currently affiliated with The Division of Cancer Control and Population Sciences, National Cancer Institute, National Institutes of Health, Bethesda, Maryland.

Noel S. Weiss, MD, DrPH (University of Washington, Seattle, Washington), Joe V. Selby, MD (Division of Research, Kaiser Permanente Medical Care Program, Oakland, California), and Nicholas P. Jewell, PhD (University of California, Berkeley, California) provided extensive methodological consultation on the design and analysis of this study.

Funding for this project came from the Department of Quality and Utilization and from the Innovations Program of the Kaiser Permanente Medical Care Program, Oakland, California, Grant Numbers 950062 and 960032.

An abstract of this work was presented at the 2001 Annual Meeting of The American College of Obstetricians and Gynecologists and was awarded second place for original research.

PII S0029-7844(02)02454-7

Received February 22, 2002. Received in revised form April 29, 2002. Accepted May 2, 2002.

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