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(Radiology. 2000;216:444-449.)
© RSNA, 2000

Genitourinary Imaging

Prediction of Deep Myometrial Invasion in Patients with Endometrial Cancer: Clinical Utility of Contrast-enhanced MR Imaging-A Meta-analysis and Bayesian Analysis1

Kathrin A. Frei, MD, Karen Kinkel, MD, Harald M. Bonél, MD, Ying Lu, PhD, Charles Zaloudek, MD and Hedvig Hricak, MD, PhD

1 From the Departments of Radiology (K.A.F., K.K., H.M.B., Y.L., H.H.) and Pathology (C.Z.), the University of California, San Francisco. From the 1999 RSNA scientific assembly. Received August 6, 1999; revision requested September 29; revision received October 28; accepted November 2. Address correspondence to H.H., Memorial Sloan-Kettering Cancer Center, 1275 York Ave, New York, NY 10021.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
 REFERENCES
 
PURPOSE: To determine if, in a patient with an endometrial cancer, in addition to the knowledge of tumor grade, preoperative magnetic resonance (MR) imaging findings contribute to treatment stratification and specialist referral.

MATERIALS AND METHODS: By using a MEDLINE literature search and institutional pathology reports, pretest probabilities for myometrial invasion were correlated with tumor grade. Likelihood ratios (LRs) were obtained through summary receiver operating characteristics.

RESULTS: The mean pretest probabilities of deep myometrial invasion were derived from seven articles (1,875 patients) and from 125 institutional pathology reports. LRs for the prediction of myometrial invasion with contrast-enhanced MR imaging were derived from nine studies (742 patients); positive and negative LRs were 10.11 and 0.1, respectively. The mean weighted pretest probabilities of deep myometrial invasion in patients with tumor grades 1, 2, or 3 were 13%, 35%, or 54%, respectively. Posttest probabilities of deep myometrial invasion for grades 1, 2, or 3 increased to 60%, 84%, or 92%, respectively, for positive and decreased to 1%, 5%, or 10%, respectively, for negative MR imaging findings.

CONCLUSION: Use of contrast-enhanced MR imaging significantly affects the posttest probability of deep myometrial invasion in patients with all grades of endometrial cancer and could be used to select patients for specialist referral.

Index terms: Uterine neoplasms, 854.32, 854.3231, 854.324 • Uterine neoplasms, MR, 854.12143 • Uterus, MR, 854.12143


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
 REFERENCES
 
Endometrial cancer is the most common gynecologic malignancy in the female pelvis, with an estimated 37,400 new cases diagnosed per year (1). In 1988, the International Federation of Gynecology and Obstetrics (FIGO) adopted a surgicopathologic system for the staging of endometrial adenocarcinoma (Table 1) (2). The rationale behind the change from the clinical to the surgicopathologic staging system was based on the inaccuracy of clinical staging and on the subsequent limitations of treatment planning (3).


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  		TABLE 1. 1988 FIGO Staging System for Endometrial Cancer
 
The histologic tumor grade and the depth of myometrial invasion in patients with endometrial cancer correlate strongly with the prevalence of lymph node metastasis and with patient survival (3). Tumor grade is the most commonly used prognostic factor that guides treatment decisions and surgical planning. Because of the higher prevalence of lymph node metastases in patients with grade 3 carcinomas, these patients are more likely to undergo surgical lymph node assessment than patients with grade 1 endometrial carcinoma. Patients with grade 1 or grade 2 carcinoma represent a clinical challenge and a treatment dilemma.

In most institutions, patients with more than 50% myometrial invasion are considered for further surgical staging, which includes pelvic and paraaortic lymphadenectomy, and therefore need referral to a specialist or need a gynecologic oncologist "standing by." A variety of radiologic and nonradiologic pre- and intraoperative procedures, which include ultrasonography (US) (4), computed tomography (CT) (5), magnetic resonance (MR) imaging (6), frozen section acquisition (7–9), and intraoperative gross estimation of the uterus (10), have been used to assess the depth of myometrial invasion. Results of a recent meta-analysis (11) showed that, in the preoperative assessment of myometrial invasion, contrast material-enhanced MR imaging in the pelvis was substantially better than US, CT, and nonenhanced MR imaging. Our study was undertaken to determine if, in a patient with a histologic diagnosis of endometrial cancer, in addition to the knowledge of tumor grade, findings of preoperative MR imaging contribute to treatment stratification and to referral to a specialist.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
 REFERENCES
 
Study Design
The pretest probabilities for deep myometrial invasion in patients with endometrial cancer were assessed by performing a meta-analysis. Posttest probabilities for deep myometrial invasion after contrast-enhanced MR imaging were obtained through Bayesian analysis.

Meta-Analysis
A comprehensive search of English-language articles and English-language abstracted studies of human subjects was performed through the MEDLINE database by combining the following key words: "endometrial carcinoma," "myometrial invasion," and "histologic grade." The search extended for data published from January 1975 to February 1999. To identify additional relevant references, the reference lists of the retrieved articles were checked manually. To include unpublished data, the database of the department of pathology was searched with the key words "total abdominal hysterectomy" and "endometrial carcinoma" for January 1989–December 1998.

The following inclusion criteria were used to select articles that reported on the pretest probabilities of deep myometrial invasion: (a) uniform standard of reference: depth of myometrial invasion assessed with histologic specimen from the uterus obtained at surgery, (b) data on myometrial invasion presented separately for each histologic tumor grade, and (c) data or subset of data published not more than once. If only a subset of patients in an article met the inclusion criteria, that subset was included in the analysis.

Among 373 pathology reports retrieved with the keyword search, the diagnosis of primary endometrial cancer and total abdominal hysterectomy were found in 170 patients. Data on tumor grade and on the depth of myometrial invasion were recorded.

Two physicians (K.A.F. and H.M.B.) abstracted the data from each article and from the pathology reports. When disagreement occurred, a third physician (K.K.) reviewed the article, and the disagreement was resolved in conference. The readers were not blinded to the origin of the publication, to the journal, or to the year of publication.

The following data were recorded for each article (Table 2): (a) the depth of myometrial invasion in each grade, (b) sample size, (c) year of publication, (d) stage distribution according to FIGO staging guidelines or to clinical or surgical staging, (e) percentage of histologic types of endometrial cancer other than endometrioid adenocarcinoma, and (f) type of hospital (community hospital vs university medical center) from which published data were obtained. For a, authors of articles published before 1988 divided the depth of myometrial invasion into thirds (inner, middle, and outer) in accordance with the FIGO staging system of 1971. Authors of study findings published after 1988 addressed the depth of myometrial invasion in "middles" (<50% or >=50% myometrial invasion). For homogeneity in data presentation, invasion of the middle third (33%–66% of patients) was categorized as deep (>50%) myometrial invasion. Therefore, the interpretation was based on the fact that pelvic lymph node metastases were found in 33% of patients with middle-third myometrial invasion (3). The 5-year survival rate in patients with more than one-third myometrial invasion is reported to be 58%, compared with 86% in patients with less than one-third myometrial invasion (12).


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  		TABLE 2. Data Abstraction
 
The weighted mean proportion of deep myometrial invasion, calculated by using the inverse of the variances, was used to determine the pretest probabilities of deep myometrial invasion in patients with grade 1, grade 2, or grade 3 endometrial cancer.

To test for heterogeneity among the included studies, we performed a subgroup analysis. We also analyzed whether the year of publication, the hospital type, the stage distribution, or the percentage of more aggressive histologic types of adenocarcinoma, such as clear cell or papillary serous, could be used to explain the differences in results among the included articles.

Bayesian Analysis and Clinical Utility
Positive and negative likelihood ratios (LRs) characterize the clinical utility of a test and are used to estimate the posttest probability of disease by means of Bayesian analysis. LRs for contrast-enhanced MR imaging with positive or negative findings were obtained from the Q* point of a summary receiver operating characteristic curve that was published in a recent meta-analysis (11) that included nine studies (11,13–21). The formula for a positive LR is sensitivity/(1 - specificity) and for a negative LR is (1 - sensitivity)/specificity. The Q* point of a summary receiver operating characteristic curve indicates the point where sensitivity and specificity are equal. Therefore, with a Q* point equal to 0.91, the positive LR was 10.11 (0.91/[1.0 - 0.91]) and the negative LR was 0.1 ([1.0 - 0.91]/0.91)(11).

The MR imaging posttest probabilities for deep myometrial invasion were calculated for each grade. The posttest probability was calculated first by converting the pretest probability into pretest odds by means of odds = probability/(1 - probability). Then, posttest odds were calculated by multiplying the pretest odds with the LR. The posttest odds were converted into probabilities by using probability = odds/(odds + 1). Since an LR of 1.0 indicates that the posttest probability is not greater than the pretest probability, clinically useful tests should have a high positive LR (>5.0, "good for confirming disease") and a low negative LR (<0.2, "good for ruling out disease") (22). The validations of the posttest probabilities were derived by using an approximation formula based on Taylor expansion (23).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
 REFERENCES
 
Meta-analysis
Seven studies in which investigators reported on the frequency of deep myometrial invasion were found through the literature search. Two of the seven studies were excluded because the depth of myometrial invasion was not given for each tumor grade. Five studies published between 1980 and 1996, in which 1,875 patients were reported on, met the inclusion criteria and were used for the meta-analysis (3,10,24–26). In addition, we included the histologic findings in 125 institutional pathology reports. Among the 170 patients with a diagnosis of endometrial cancer, 45 were excluded because their histologic tumor type differed from that of endometrioid adenocarcinoma. Data for deep myometrial invasion were available in a total of 2,000 patients. Table 2 gives the characteristics evaluated for all of the studies evaluated.

As shown in Table 3, 41% of all patients had grade 1, 41% had grade 2, and 18% had grade 3 endometrial cancer. The pretest probabilities for deep myometrial invasion were 13% (95% CI: 11%, 15%) in grade 1, 35% (95% CI: 31%, 38%) in grade 2, and 54% (95% CI: 49%, 59%) in grade 3 (Table 4). Covariate analysis results showed that the year of publication, the clinical or surgical staging, the hospital type, and the distribution of histologic types of adenocarcinoma did not influence the results.


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  		TABLE 3. Results for Deep Myometrial Invasion in Patients with Endometrial Cancer

 

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  		TABLE 4. Pretest Probabilities for Deep Myometrial Invasion and Posttest Probabilities with Contrast-enhanced MR Imaging
 
Bayesian Analysis
The LRs for the prediction of deep myometrial invasion with contrast-enhanced MR imaging were derived from nine studies (742 patients) (11). The positive LR for contrast-enhanced MR imaging was 10.11, and the negative LR was 0.1. As shown in Table 4, the posttest probabilities of contrast-enhanced MR imaging used to diagnose deep myometrial invasion were 60% (95% CI: 53%, 66%) in grade 1, 84% (95% CI: 81%, 87%) in grade 2, and 92% (95% CI: 90%, 94%) in grade 3. For grades 1, 2, and 3, the posttest probabilities for contrast-enhanced MR imaging used to exclude deep myometrial invasion were 1% (95% CI: 0%, 8%), 5% (95% CI: 2%, 8%), and 10% (95% CI: 8%, 12%), respectively. As compared with tumor grade alone, findings of contrast-enhanced MR imaging in patients with biopsy-proved endometrial cancer substantially affect the posttest probability of deep myometrial invasion.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
 
It was estimated that 37,400 new cases of endometrial cancer would be diagnosed in the United States in 1999 (1). For a patient with endometrial cancer, the presence of deep myometrial invasion is an important prognostic factor that strongly affects treatment planning and prognosis. The depth of invasion is a highly important factor that can be used to predict nodal metastasis (26). The reported 5-year survival rate in patients with deep myometrial invasion or with grade 3 endometrial cancer is 58%–59% compared with 89% for patients with grade 1 endometrial cancer (10,12,27).

Patients with greater than 50% myometrial invasion have a six- to sevenfold higher prevalence of pelvic and paraaortic lymph node metastases and of advanced surgical stage when compared with patients with less than 50% myometrial invasion (25,26,27). Patients with deep myometrial invasion therefore should be considered for more aggressive surgical staging, which includes pelvic and paraaortic lymphadenectomy (10). To our knowledge, there is no consensus on how to select patients preoperatively who might benefit from more aggressive surgical staging.

As patients with grade 2 or grade 3 endometrial cancer are at higher risk for deep myometrial invasion, intraoperative frozen sections are obtained (8,9) or gross inspection of the uterus (10) usually is performed to assess the depth of myometrial invasion. On the basis of these findings, the surgeon decides whether, at the time of hysterectomy, lymphadenectomy should be performed. If surgery is performed by a general gynecologist, who usually does not perform lymphadenectomy, patients with a histopathologic diagnosis of deep myometrial invasion either receive inadequate staging or require a second surgery for lymph node dissection and for complete staging (3). The initial treatment in a patient with cancer offers the best opportunity for cure (28); therefore, accurate preoperative assessment of the depth of myometrial invasion is very important, as it will be used to select patients who might benefit from referral to a subspecialist.

Among the imaging modalities that have been proposed for the evaluation of myometrial invasion, contrast-enhanced MR imaging has a substantially higher sensitivity and specificity than endovaginal US or CT (11). Figure 1 is a contrast-enhanced MR image of superficial myometrial invasion in a patient with endometrial cancer. In comparison, Figure 2 is a contrast-enhanced MR image in a patient with endometrial cancer that demonstrates deep invasion.



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  		Figure 1. Sagittal T1-weighted gradient-recalled-echo MR image of endometrial cancer in a 61-year-old patient. The image was acquired 1 minute after the intravenous injection of gadopentetate dimeglumine. The endometrial tumor can be well appreciated as it expands the endometrial cavity. Superficial invasion (arrow) is depicted, as well.

 


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  		Figure 2. Sagittal T1-weighted gradient-recalled-echo MR image of endometrial adenocarcinoma in a 42-year-old woman. The tumor is in the lower uterine segment. The dynamic gadolinium-enhanced image, acquired 1 minute after contrast material injection, shows deep myometrial invasion (arrow) in the posterior myometrial wall.

 
As the tumor grade is known before surgery (through biopsy or curettage) and correlates with the depth of myometrial invasion, the purpose of our study was to evaluate the incremental value of contrast-enhanced MR imaging in the preoperative assessment of the depth of myometrial invasion for each grade of endometrial cancer and to determine if MR imaging findings contribute to treatment stratification and specialist referral. The conflicting reports in the literature on the frequency of deep myometrial invasion led to the choice of a meta-analysis to achieve the most accurate summary of pretest probability for each tumor grade. The results of this meta-analysis confirmed the expected high frequencies of deep myometrial invasion in patients with grade 2 or grade 3 disease. However, patients with grade 1 endometrial cancer had a 13% weighted mean frequency of deep myometrial invasion. This value is higher than the approximate 7% reported by Boronow et al (3) and by Larson et al (10). The higher frequency of deep myometrial invasion in patients with grade 1 adenocarcinoma can be attributed in part to differences in the staging system before and after 1988.

In addition, we attempted to identify reasons for heterogeneity between study results. The subgroup analysis, however, did not demonstrate any differences in the results when the years of publication, the types of institution, the stage distributions, or the percentages of more aggressive histologic types of adenocarcinoma (such as clear cell or papillary serous) were compared. The results of this meta-analysis are likely to be valid, as it has been shown that multiple smaller studies, when combined in a meta-analysis, have results that are comparable with the results of large randomized trials (29).

By considering the histologic grade as the main prognostic factor for the decision to perform lymphadenectomy, 13% of patients with grade 1 endometrial cancer would be designated as having a stage lower than their actual stage. Forty-one percent of the 37,400 newly diagnosed endometrial cancers each year are grade 1; therefore, about 2,000 patients would not be treated optimally. By assuming that all patients with grade 3 cancer would undergo lymphadenectomy, 46% of patients would undergo a more invasive surgery than is necessary. This results in a higher surgical risk, a longer recuperation period, and a higher morbidity rate (28).

The clinical usefulness of an examination is expressed well by the magnitude of the LR, which, through Bayesian analysis, relates directly to the degree of change in the predictive value with the application of the examination. The positive LR of 10.11 in our study means that contrast-enhanced MR imaging is clinically useful in diagnosing deep myometrial invasion. A negative LR of 0.1 means that contrast-enhanced MR imaging is clinically useful in excluding deep endometrial invasion (22).The results of this Bayesian analysis show that, in patients with grade 1 or grade 2 endometrial cancer, a lack of deep myometrial invasion at preoperative contrast-enhanced MR imaging can be used to exclude deep invasion reliably. Such a knowledge and confidence in MR imaging might decrease the need for a frozen section to be obtained or for an oncologist to be standing by during surgery. This change in practice therefore may reduce the cost and time of surgery. In patients with a grade 3 endometrial cancer, a positive examination result would increase the probability for deep myometrial invasion from 54% to 92%. With this preoperative information, there would be very little justification for routinely obtaining frozen sections during surgery. Furthermore, a negative examination result indicates that the patient does not need lymphadenectomy and could therefore undergo surgery by a general gynecologist. In patients with difficult access to a specialist, contrast-enhanced MR imaging can be an option for treatment stratification.

In conclusion, the results of this study provide evidence that, in patients with biopsy-proved endometrial cancer, preoperative contrast-enhanced MR imaging should be considered as the preferred diagnostic adjunct for clinical treatment planning and for specialist referral.


   FOOTNOTES
 
Abbreviations: FIGO = International Federation of Gynecology and Obstetrics, LR = likelihood ratio

Author contributions: Guarantors of integrity of entire study, K.A.F., H.H., Y.L.; study concepts, K.A.F., K.K., H.H.; study design, K.A.F.; definition of intellectual content, K.A.F., K.K., H.H.; literature research, K.A.F., H.M.B.; data acquisition, K.A.F., K.K., H.M.B., C.Z.; data analysis, K.A.F., K.K., Y.L.; statistical analysis, Y.L., manuscript preparation, K.A.F.; manuscript editing, K.A.F., K.K., H.M.B., H.H.; manuscript review, H.H., C.Z.


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 MATERIALS AND METHODS
RESULTS
DISCUSSION
 REFERENCES
 

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