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Role of Imaging in Pretreatment Evaluation of Early Invasive Cervical Cancer: Results of the Intergroup Study American College of Radiology Imaging Network 6651–Gynecologic Oncology Group 183

From the Department of Radiology, and the Gynecology Service/Department of Surgery, Memorial Sloan-Kettering Cancer Center, New York, NY; Center for Statistical Sciences, Brown University; Department of Diagnostic Imaging, Brown University/Rhode Island Hospital, Providence, RI; Department of Radiology, University of Miami Medical School, Miami; Division of Gynecologic Oncology, H. Lee Moffitt Cancer Center, Tampa, FL; Department of Radiology and Department of Medical Oncology, Mayo Clinic College of Medicine, Rochester, MN; Department of Radiology, University of Pennsylvania Health System; Department of Radiology, Thomas Jefferson University Hospital, Philadelphia, PA; Mallinckrodt Institute of Radiology, Washington University School of Medicine, St Louis, MO; Division of Diagnostic Imaging, The University of Texas M.D. Anderson Cancer Center, Houston, TX; Mount Carmel Health System; Department of Radiology, Ohio State University Medical Center, Columbus, OH

Address reprint requests to Hedvig Hricak, MD, PhD, Department of Radiology, Memorial Sloan-Kettering Cancer Center, 1275 York Ave, Room c-278, New York, NY 10021; e-mail: muellnea{at}mskcc.org

	ABSTRACT

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION Authors' Disclosures of... REFERENCES

 
PURPOSE: To compare magnetic resonance imaging (MRI) and computed tomography (CT) with each other and to International Federation of Gynecology and Obstetrics (FIGO) clinical staging in the pretreatment evaluation of early invasive cervical cancer, using surgicopathologic findings as the reference standard.

PATIENTS AND METHODS: This prospective multicenter clinical study was conducted by the American College of Radiology Imaging Network and the Gynecologic Oncology Group from March 2000 to November 2002; 25 United States health centers enrolled 208 consecutive patients with biopsy-confirmed cervical cancer of FIGO stage IB who were scheduled for surgery based on clinical assessment. Patients underwent FIGO clinical staging, helical CT, and MRI. Surgicopathologic findings constituted the reference standard for statistical analysis.

RESULTS: Complete data were available for 172 patients; surgicopathologic findings were consistent with FIGO stages IA to IIA in 76% and stage IIB in 21%. For the detection of advanced stage ( IIB), sensitivity was poor for FIGO clinical staging (29%), CT (42%), and MRI (53%); specificity was 99% for FIGO clinical staging, 82% for CT, and 74% for MRI; and negative predictive value was 84% for FIGO clinical staging, 84% for CT, and 85% for MRI. MRI (area under the receiver operating characteristic curve [AUC], 0.88) was significantly better than CT (AUC, 0.73) for detecting cervical tumors (P = .014). For 85% of patients, FIGO clinical staging forms were submitted after MRI and/or CT was performed.

CONCLUSION: CT and MRI performed similarly; both had lower staging accuracy than in prior single-institution studies. Accuracy of FIGO clinical staging was higher than previously reported. The temporal data suggest that FIGO clinical staging was influenced by CT and MRI findings.

	INTRODUCTION

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Cervical carcinoma is the third most common gynecologic malignancy in the United States, with 10,370 new cases and 3,710 deaths expected in 2005.¹ Accurate cervical cancer staging is crucial for appropriate treatment selection and treatment planning. Patients with cervical cancer of International Federation of Gynecology and Obstetrics (FIGO) stage IIA or lower can be treated with radical hysterectomy and pelvic lymphadenectomy, combined radiation-chemotherapy, or in some cases, radiation therapy alone.² Patients with cervical cancer stage IIB or higher (documented parametrial disease) are best treated by a combination of radiotherapy and chemotherapy.

Cervical cancer is the only gynecologic cancer still clinically staged. Staging is based on 1994 clinical FIGO criteria (summarized in Table 1 ³). These include findings from physical examination, colposcopy, lesion biopsy, radiologic studies (eg, chest radiography, intravenous urography, and barium enema), and endoscopic studies (eg, cystoscopy, sigmoidoscopy).⁴ Compared with surgical staging, FIGO clinical staging has been shown to result in understaging of up to 20% to 30% in stage IB, up to 23% in stage IIB, and almost 40% in stage IIIB, as well as overstaging of approximately 64% in stage IIIB.^5-9

The primary aim of this interdisciplinary multicenter American College of Radiology Imaging Network/Gynecologic Oncology Group (ACRIN/GOG) clinical study was to compare the levels of diagnostic performance of MRI and CT with each other and with FIGO clinical staging in the pretreatment evaluation of invasive cancer of the cervix, using surgicopathologic findings as the reference standard. A set of minimum standards was defined for imaging equipment, protocols, and reader qualifications, but a broad range representing current practice was considered acceptable. Therefore, compared with the results of prior single-institution reports, the results of this study should more accurately reflect the role and value of imaging in current clinical practice in the United States.

	PATIENTS AND METHODS

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION Authors' Disclosures of... REFERENCES

 
This prospective, multicenter, interdisciplinary clinical study was conducted jointly by the ACRIN and the GOG.

Patients
Consecutive patients with biopsy-confirmed cervical cancer of FIGO clinical stage IB who were scheduled for surgery based on clinical assessment were enrolled. Reference information was derived from the pathologic examination of surgical specimens or from surgical notes supplemented by intraoperative biopsy when hysterectomy was aborted.

Patient Inclusion Criteria
The patient inclusion criteria included biopsy-confirmed invasive cervical cancer (including invasive squamous cell carcinoma, adenocarcinoma, or adenosquamous carcinoma), for which surgery was intended and for which a FIGO clinical stage of at least IB1 was assigned before imaging; willingness to sign a study-specific informed consent form and to undergo both contrast-enhanced CT and MRI preoperatively; and lack of prior treatment for cervical cancer. In addition, only patients whose surgery was to be performed at the participating institution could be enrolled. The interval between the first protocol imaging study and surgery could not exceed 6 weeks, and pathology slides (tumor type and grade) had to be available for review at the participating institution.

Patient Exclusion Criteria
Patients unwilling or unable to undergo contrast-enhanced CT or MRI were excluded from the study, including any patient with a contraindication to CT or MRI. Also excluded were pregnant patients; patients who, because of age, general medical or psychiatric condition, or physiologic status unrelated to the presence of cervical cancer could not give informed medical consent or were not considered surgical candidates; patients who had had previous medical, surgical, or radiation treatment for invasive cervical cancer; and patients scheduled for a loop electrosurgical excision procedure or only a cone biopsy.

Participating Site Selection Criteria
Each participating institution was required to submit a protocol-specific application to ACRIN; be a GOG participant with a proven record of 20 surgical cases of gynecologic cancer per year; have 1.5-T MRI (any manufacturer) and helical CT equipment (any manufacturer); and have at least two radiologists, a gynecologic oncologist, and a pathologist designated to work on the study, who were adequately qualified and committed to the study's goals.

Patient Accrual
Consecutive patients were recruited from the gynecologic oncology clinics of participating institutions. A patient's eligibility for the study was assessed by the gynecologic oncologist, who determined the appropriateness of the primary surgical therapy and contacted the institutional GOG or ACRIN research assistant. Patients were enrolled before surgical exploration and after signing a study-specific informed consent form.

Institutional Review Board Approval and Informed Consent
All institutions had study-specific institutional review board approval. Copies of each institution's institutional review board approval notice and study-specific consent form were on file at ACRIN headquarters before patient registration.

Clinical Assessment
Pre-enrollment evaluation included a standard pelvic examination; review of the pathology slides; and, as clinically indicated, any FIGO-recommended diagnostic tests, which could include examination under anesthesia. Studies performed during the patients' FIGO diagnostic work-ups were recorded and subsequently tabulated. The sequence of examinations used for pre-enrollment FIGO clinical staging was modeled according to local standards of care and was left to the discretion of referring gynecologic oncologists. However, FIGO clinical staging was to be based solely on conventional FIGO-recommended diagnostic tests.

The decision for surgical treatment was to be based on pre-enrollment FIGO assessment. The results of the MRI and CT examinations were communicated to the referring gynecologic oncologist. Imaging findings of suspected parametrial invasion were not to influence the treatment decision, as the accuracy of CT and MRI for the assessment of parametrial invasion had not been proven at the time the study was designed. However, imaging findings suspicious for metastatic involvement of lymph nodes (lymph node size greater than 1 cm in the short axis) were permitted to influence the decision to perform lymph node biopsy or lymphadenectomy and, potentially, to cancel plans for radical hysterectomy in accordance with the accepted standard of care.

Imaging Technique
All MRI and CT examinations met or exceeded standards agreed on by the investigators. Some patients had pre-enrollment CT or MRI. At the discretion of the site radiologic investigator, outside CT or MRI studies were accepted if they met the established standards.

CT
CT was performed using a single-row helical/spiral scanner with rapid scanning in a helical/spiral mode with subsecond scan times. Oral contrast was used, consisting of 1,000 mL 3% diatrizoate sodium or equivalent, usually given as divided doses (250 mL) over 60 to 90 minutes, with the last dose 10 to 15 minutes before CT examination. The use of contrast enema to opacify the rectosigmoid colon was left to the discretion of each site. Intravenous contrast medium was used in all cases, consisting of a total of 120 to 150 mL of 60% iodinated contrast medium delivered by power injector at 2.0 to 3.0 mL/sec. The scanning began at the symphysis pubis and was performed during suspended respiration using collimation of 5 mm or less, 5-mm reconstruction at 5 mm or less, and appropriate table speed.

MRI
All MRI studies were performed on 1.5-T MRI units with fast spin-echo (FSE) and phased array techniques involving pelvic or torso phased-array coils. The minimally required MRI sequences included (A) localizer, sagittal, or coronal plane; (B) sagittal plane of section, FSE T2-weighted image; (C) axial plane of section, FSE T2-weighted image; (D) axial plane of section, T1-weighted image extending from the symphysis pubis to above the renal hilum.

The equipment and protocol details varied, as did the use of dynamic or static postcontrast imaging, which was left to the discretion of the site investigators. For all of the sequences, the field of view varied between 20 and 28 cm; slice thickness was 5 mm or less; matrix was 256 x 192 or better; and number of signals averaged was two or more.

Image Analysis
At each participating institution, each radiologist designated to work on the study read either only MRI studies or only CT studies. Interpretation was always performed at the institution where the imaging took place. Individual imaging findings relevant for staging of cervical cancer were recorded on standardized data forms; they included tumor presence, tumor location (endocervix versus external os), tumor size, stromal invasion, primary tumor extension to the vagina, parametrium or adjacent tissues, and presence of lymph node metastases. At the end of the imaging evaluation session, overall stage was recorded using both FIGO and TNM classification criteria.

Surgical Pathology
Surgicopathologic findings (the data from the surgical report and the pathologic analysis of specimens) comprised the reference standard for stage determination. At the end of the surgical procedure, the surgeon completed the surgical data form. Data from the pathologic examination of specimens were collected from the GOG pathology template, and both FIGO and TNM stage classifications were recorded. Centralized pathology rereview of the slides was not done.

Data Collection and Statistical Analysis
Data were collected, managed and analyzed by the Biostatistics and Data Management Center of ACRIN. The primary aim of the protocol was to use the pooled data across sites to compare CT, MRI, and clinical FIGO staging on the basis of diagnostic performance as measured by sensitivity, specificity, positive predictive value (PPV) and negative predictive value (NPV). Staging determinations were dichotomized as stage IIA or lower versus stage IIB or higher for purposes of the primary analysis. Thus "positive" was defined as stage IIB or higher, and "negative," as all other stages. This choice of threshold corresponds to the primary staging factor for choosing candidates for radical hysterectomy; namely, the assessment of the parametria. For each modality, 95% CIs were estimated for each measure of diagnostic performance. Sensitivities and specificities were compared using McNemar's test. Predictive values were compared using a score test.¹⁶

Subsequently, the threshold for dichotomizing stages was varied, and estimates of sensitivity, specificity, PPV, and NPV of diagnostic performance were recomputed for each threshold. We assessed the degree of agreement in the determination of stage between each modality and the reference standard. For each pair of stage classifications, we computed percentages of exact and near-exact (differing by one category) matches, and also computed unweighted and weighted statistics and corresponding 95% CIs.

To evaluate the detection of cervical involvement on CT and MRI, receiver operating characteristic (ROC) analysis was carried out using the ROCKIT software.¹⁷ The test result was the radiologist's degree of suspicion for cervical involvement recorded on a five-point ordinal categorical scale, ranging from category 1 (cancer not identified on imaging) to category 5 (cancer definitely identified on imaging) on the interpretation form for each modality. A bivariate binormal ROC model was used to estimate and compare areas under the ROC curves, accounting for the correlation in the data due to the paired tests.

Although lymph node metastases do not play a role in FIGO clinical staging, they play an integral role in TNM staging. Therefore, we also calculated the sensitivity and specificity of MRI and CT for detecting lymph node involvement and compared them via McNemar's test.

Sample Size Considerations
Initially, 465 women were projected to enroll in this study throughout a period of 18 months. We expected complete data on 440 cases. We also expected that approximately 29% of cases would have a stage of IIB or higher. Based on the literature review, we assumed the sensitivity, specificity, and negative predictive value of FIGO clinical staging to be 17%, 99%, and 75%, respectively, the corresponding figures for MRI to be approximately 75%, 90%, and 90%, and the corresponding figures for CT to be approximately 60%, 85%, and 84%. The total sample size was determined to ensure adequate precision for study goals.

Cessation of Patient Accrual
The study commenced in March 2000 and, in consultation with the Data and Safety Monitoring Committee of ACRIN and GOG, was closed to further accrual in November 2002 with 208 patients accrued. Practice patterns evolved during the period in which the study was designed and conducted, resulting in notably increased reliance on CT and MRI as part of the diagnostic work-up for cervical cancer staging. The change in practice patterns and slow patient accrual were the primary reasons for terminating the study. The Data and Safety Monitoring Committee acknowledged that the reduction in the sample size implied a commensurate reduction in statistical power and precision of estimates.

	RESULTS

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Patient Cohort and Tumor Stage
Between March 1, 2000, and November 11, 2002, 25 academic and community health centers enrolled a total of 208 patients in the study. Thirty-six patients were excluded from the final data analysis (Fig 1), including 13 who did not have surgery for the following reasons: disease deemed too extensive on imaging (n = 9); medical contraindications to surgery (n = 1); surgery refused by patient (n = 1); radiation and/or chemotherapy was received instead (n = 2). Table 2 summarizes the patient demographics, and Table 3 presents the distribution of patient tumor characteristics. There were no significant differences between the eligible and analysis sets of patients in terms of demographics or clinical characteristics (data not shown).

View larger version (35K): [in this window] [in a new window]   Fig 1. Patient flowchart. Of 208 patients enrolled in the study, nine were subsequently deemed ineligible; of the remaining 199 patients, 172 (86%) had complete data sets for inclusion in the data analysis. CT, computed tomography; MRI, magnetic resonance imaging; FIGO, International Federation of Gynecology and Obstetrics.

The distribution of clinical FIGO stages is reported in Table 4. Seventy-six percent (130 of 172) of women had surgico-pathologic findings consistent with a FIGO stage in the range of IA to IIA and 21% (36 of 172) had surgicopathologic findings consistent with a FIGO stage of IIB or higher (Table 5).

Estimated sensitivities were poor for FIGO clinical staging (29%; 95% CI, 15% to 46%), CT (42%; 95% CI, 26% to 59%) and MRI (53%; 95% CI, 35% to 70%; Table 6). The specificities were 99% (95% CI, 96% to 100%) for FIGO clinical staging, 82% (95% CI, 75% to 88%) for CT and 75% (95% CI, 67% to 83%) for MRI. There was no significant difference between the sensitivities of CT and MRI (95% CI, –0.31 to 0.08; P = .34) or between their specificities (95% CI, –0.15 to 0.01; P = .09).

FIGO clinical staging data were likely influenced by imaging findings, as 85% of patients (147 of 172) had their final FIGO clinical staging results submitted after CT or MRI was done. Furthermore, all patients were considered surgical candidates at the time of study enrollment.

Ability of Cross-Sectional Imaging to Detect Tumor
In the detection of cervical tumor, MRI (area under the ROC curve [AUC], 0.88) performed significantly better than CT (AUC, 0.73; P = .014; Fig 2).

View larger version (12K): [in this window] [in a new window]   Fig 2. Plots of receiver operating characteristic (ROC) curves for the assessment of cervical involvement by magnetic resonance imaging (MRI) and computed tomography (CT). For each modality, the estimated area under the ROC curve is reported. MRI was significantly better than CT for detecting cervical tumor, as measured by the respective areas under the ROC curves (AUC).

When the threshold for "advanced stage" was varied from stage IIB (the threshold used in the primary analysis), the estimates of diagnostic performance of CT and MRI changed accordingly (Figs 3 and 4). Sensitivity decreased and specificity increased as the stage threshold increased. Similarly, PPV decreased and NPV increased as the stage threshold increased.

View larger version (8K): [in this window] [in a new window]   Fig 3. Sensitivity and specificity of computed tomography (CT) and magnetic resonance imaging (MRI) for different stage thresholds. When the threshold was set at IA (so that the diagnostic task would be to detect stages IB or higher), CT and MRI had high sensitivity (0.80; 0.73 to 0.86; and 0.90; 0.84 to 0.94, respectively) and low specificity (0.54; 0.25 to 0.81; and 0.46; 0.19 to 0.75, respectively). Sensitivity decreased and specificity increased as the stage threshold increased.

View larger version (9K): [in this window] [in a new window]   Fig 4. Positive and negative predictive values of computed tomography (CT) and magnetic resonance imaging (MRI) for different stage thresholds. When the threshold was set at stage IA, CT and MRI had high positive predictive value (PPV; 0.95; 0.90 to 0.98 for both modalities) and low negative predictive value (NPV; 0.19; 0.08 to 0.35; and 0.27; 0.11 to 0.50; respectively). PPV decreased and NPV increased as the stage threshold increased.

Detection of Bladder Involvement
There were six cases with tumor present in the bladder, as assessed either by pathology examination of surgically obtained specimens (two cases) or by surgical assessment without resection (four cases). MRI detected two of these cases, and CT did not detect any of these cases.

Detection of Lymph Node Involvement
Fifty-five patients (32%) had documented positive lymph nodes at surgery. Of these patients, 14 had positive para-aortic nodes, seven had positive common iliac nodes (with negative or unexamined para-aortic nodes), and 34 had other positive nodes (with negative or unexamined positive para-aortic and common iliac nodes). In detecting lymph node involvement, the specificity of MRI was significantly better than that of CT (P = .01), but both modalities had very low sensitivity (Table 7).

	DISCUSSION

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Clinical FIGO staging achieved high specificity (99%), positive predictive value (91%) and negative predictive value (84%) in our study. Nevertheless, although at enrollment all patients were considered to have a clinical FIGO stage of IB or IIA and were scheduled for surgery, 36 (21%) of the 172 patients included in the final data analysis had a proven pathological stage greater than IIA and 55/172 (32%) had malignant lymph nodes at surgery.

The conventional diagnostic FIGO-recommended tests were used at very low rates in our study (for example, proctoscopy or sigmoidoscopy was performed in only 9%, intravenous urography in only 1%, and lymphangiography and barium enema in 0% of patients).²⁷ These low rates of usage are consistent with the data presented in a patterns of care study by Russell et al published in 1996; that study found that the use of conventional FIGO clinical staging tests in the United States had been declining since the 1980s and suggested that conventional FIGO clinical staging methods were increasingly being replaced by a single comprehensive CT or MR imaging examination providing evaluation of all morphologic cervical cancer prognostic factors (including tumor size, parametrial invasion, adjacent organ/tissue invasion, and lymph node metastasis).¹³

The temporal data from our study (dates of CT and MR imaging, of FIGO clinical tests, and of submission of final FIGO clinical staging results) provide indirect evidence that the FIGO clinical staging results recorded on the official data form could have been influenced by imaging findings from CT and MRI. This does not affect the validity of our results regarding the accuracy of CT and MRI. However, given the unusually high accuracy of FIGO clinical staging in our study, it does suggest that the inclusion of CT and/or MRI findings may result in markedly improved clinical staging.

	Authors' Disclosures of Potential Conflicts of Interest

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Although all authors completed the disclosure declaration, the following author or immediate family members indicated a financial interest. No conflict exists for drugs or devices used in a study if they are not being evaluated as part of the investigation. For a detailed description of the disclosure categories, or for more information about ASCO's conflict of interest policy, please refer to the Author Disclosure Declaration and the Disclosures of Potential Conflicts of Interest section in Information for Contributors.

Authors Employment Leadership Consultant Stock Honoraria Research Funds Testimony Other Harry J. Long III Pfizer (A); GSK (A); Genentech (A); IBM (B) GSK (A)

Dollar Amount Codes (A) < $10,000 (B) $10,000-99,999 (C) $100,000 (N/R) Not Required

	Acknowledgment

 
We thank Ada Muellner for helping to write and edit the manuscript.

	NOTES

 
Supported by original research NCI Grants U01 CA079778 and U01 CA080098.

Authors' disclosures of potential conflicts of interest are found at the end of this article.

	REFERENCES

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Submitted March 17, 2005; accepted September 22, 2005.

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