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© 2003 American Society for Clinical Oncology Value of Dual-Phase 2-Fluoro-2-Deoxy-D-Glucose Positron Emission Tomography in Cervical Cancer
From the Department of Nuclear Medicine; Department of Radiology; Division of Gynecologic Oncology, Department of Obstetrics and Gynecology; Department of Radiation Oncology; and Department of Pathology, Chang Gung Memorial Hospital and Chang Gung University; Biostatistics Consulting Center/Department of Public Health, Chang Gung University; and Institute of Nuclear Energy Research, Taoyuan, Taiwan. Address reprint requests to Chyong-Huey Lai, MD, Department of Obstetrics and Gynecology, Chang Gung Memorial Hospital, Linkou Medical Center, 5 Fu-Shin St, Kueishan, Taoyuan 333, Taiwan; e-mail: sh46erry{at}ms6.hinet.net.
Purpose: The role of positron emission tomography (PET) with fluorine-18–labeled fluoro-2-deoxy-D-glucose (FDG) in cervical cancer has not yet been well defined. We conducted a prospective study to investigate its efficacy in comparison with magnetic resonance imaging and/or computed tomography (MRI-CT). Materials and Methods: Patients with untreated locally advanced (35%) or recurrent (65%) cervical cancer were enrolled onto this study. In the first part of this study, 41 patients had a conventional FDG-PET (40 minutes after injection), and in the second part, 94 patients received dual-phase PET (at both 40 minutes and 3 hours after injection). The overall results of PET scans were compared with MRI-CT, and the two protocols of PET were also compared with each other. Lesion status was determined by pathology results or clinical follow-up. The receiver operating characteristic curve method with area under the curve (AUC) calculation was used to evaluate the discriminative power. Results: Overall (N = 135), FDG-PET was significantly superior to MRI-CT in identifying metastatic lesions (AUC, 0.971 v 0.879; P = .039), although the diagnostic accuracy was similar for local tumors. Dual-phase PET was also significantly better than the 40-minute PET (n = 94). The latter accurately recognized 70% of metastatic lesions and the former detected 90% (AUC, 0.943 v 0.951; P = .007). Dual-phase FDG-PET changed treatment of 29 patients (31%; upstaging 27% and downstaging 4%). Conclusion: This study shows that dual-phase FDG-PET is superior to conventional FDG-PET or MRI-CT in the evaluation of metastatic lesions in locally advanced or recurrent cervical cancer.
THE INTERNATIONAL Federation of Gynecology and Obstetrics (FIGO) staging system is widely accepted.1 The FIGO staging for cervical cancer is based on physical and clinical examination and simple radiologic imaging studies such as chest x-ray and intravenous pyelography. Although palpable supraclavicular lymph node (SLN) metastases could be designated as stage IVb, other metastatic lesions detected by computed tomography (CT) scan or magnetic resonance imaging (MRI), such as those in pelvic, para-aortic, or mediastinal lymph nodes (MLNs), or lung, liver, bone, and peritoneum, will not alter the FIGO stage. However, identification of metastatic sites will certainly influence treatment strategies and prognosis of the individual patient. MRI and CT rely on size criteria and morphologic changes for lesion detection, and are limited in differentiating tumor infiltration from reactive hyperplasia or posttreatment fibrosis or scarring.2–5 The fluorine-18–labeled fluoro-2-deoxy-D-glucose positron emission tomography (FDG-PET) scan gives functional imaging of metabolic processes that are increased in many malignant cells. Recently, it has been shown to be superior to MRI and/or CT for evaluation of many malignancies.6 Several investigators also considered FDG-PET useful in cervical cancer,7–12 although controversial results also have been reported.13 Discrepancies may arise from the differences in patient selection, radiotracer doses, imaging protocols, or interpretation. Most scans in previous PET studies were performed about 1 hour after tracer injection, partly because of the 110-min physical half-life of fluorine-18. This prospective study compared the efficacy of FDG-PET with MRI-CT for staging cervical cancer. In the first part of this study when 41 patients were enrolled, there were substantial false-positive and false-negative results using the conventional FDG-PET protocol (scan performed 40 minutes after injection). Dual-phase or multiphase FDG-PET has been shown to differentiate benign from malignant lesions in certain malignancies.14–19 Therefore, a second scan at 3 hours after injection was added for the second part of this study. To the best of our knowledge, the role of a delayed FDG-PET scan in cervical cancer has never before been reported.
Patients This study, which was approved by the institutional review board of our hospital, required written informed consent from all patients enrolled. Patients with histologic diagnosis of cervical carcinoma were eligible if they had any of the following criteria: were previously untreated and scheduled for definitive radiotherapy (RT), with at least one enlarged pelvic lymph node (PLN;  1.0 cm in maximal dimension) or groups of small PLNs (< 1 cm), without suspected para-aortic lymph node (PALN) metastasis or other extrapelvic lesions detected by MRI; had suspicious PALNs on MRI-CT or clinically palpable SLNs or inguinal nodes (ILNs) without other overt distant metastasis, with treatment of curative intent feasible; had histologically proven recurrent or persistent cancer after definitive RT or surgery and were willing to receive salvage therapy of curative intent; or had unexplained squamous cell carcinoma antigen or carcinoembryonic antigen elevation (squamous cell carcinoma > 2 ng/mL or carcinoembryonic antigen > 10 ng/mL on two tests 1 month apart).
CT Imaging
MRI Imaging
PET Imaging
Image Analysis
For dual-phase PET, the combination of early and late images was used to determine if the observed lesion was fixed and to calculate changes in SUV from early to late results. Films of MRI-CT were analyzed separately by an experienced radiologist who was blinded to the FDG-PET results. The five-grade scoring criteria were also used for MRI-CT image interpretation: grade 0, a normal finding; 1, visible LNs less than 0.5 cm in size, considered reactive and unrelated to metastasis; 2, any LN of length 1 cm or a little less, giving an overall equivocal impression; 3, LNs more than 1 cm in length in the short axis and/or multiple LNs (n
Study Procedures and Determination of Lesion Status
Statistical Analysis The result of a lesion observed by either FDG-PET or MRI-CT was positive with a score of 3 or 4, and negative for scores 0, 1, or 2. True-positive was defined as those patients with disease (determined with pathologic findings or an additional clinical follow-up) evaluated as positive by the imaging method. True-negative was defined as those patients whose disease was not evaluated negative and who remained disease-free at least 6 months with clinical and imaging follow-up. False-positive was defined as those patients without disease (determined with pathologic findings or an additional clinical follow-up) and either a positive FDG-PET or MRI-CT scan. False-negative was defined as those patients with disease and either a negative FDG-PET or MRI-CT scan. Sensitivity, specificity, positive-predictive value, negative-predictive value, and accuracy were calculated. The influence of FDG-PET in restaging and changing the treatment plan was also evaluated. All statistical tests were two-sided.
Between February 1, 2001 and October 31, 2002, 135 patients (mean age 56 ± 12 years; range, 28 to 87 years) were enrolled onto the study. Of these patients, 47 (35%) had newly diagnosed cervical cancer (16 with stage IB2, four with stage IIA, 15 with stage IIB, two with stage IIIA, five with stage IIIB, one with stage IVA, and four with stage IVB) and 88 (65%) had documented recurrent or persistent cervical cancer or unexplained elevation of tumor markers. The histopathology types were squamous cell carcinoma in 108 patients, adenocarcinoma in 14 patients, adenosquamous carcinoma in seven patients, small-cell carcinoma in four patients, and poorly differentiated carcinoma in two patients. Thirty-five patients (26%) had a primary site and metastatic PLNs (criteria 1); eight patients (6%) had a primary site and both metastatic PLNs and PALNs and/or ILNs (criteria 2), and four patients (3%) had a primary site and a limited distant site (eg, SLNs) detected by conventional imaging (criteria 2); 64 patients (47%) had local or pelvic recurrence with or without limited distant failure (  two sites of solitary mass or two lesions at same site) detected by conventional imaging (criteria 3), five patients (4%) had a persistent primary tumor (criteria 3), and 19 patients (14%) had unexplained tumor marker elevation after definitive treatment (criteria 4).
In the first part of the study, 41 patients had a single FDG-PET scan at 40 minutes and an MRI-CT study. Because of substantial false-positive and false-negative findings, the additional 3-hour FDG-PET scan in the subsequent 94 patients compared the efficacy of the two different PET protocols (40 minute v dual phase). All patients (n = 135) had abdominal and pelvic MRI-CT, in which peritoneum, bone (T-11 to the femoral upper shafts), liver, PALNs, PLNs and ILNs, and primary or recurrent local tumor (135 x 7 = 945 sites) were evaluated. Forty-one patients had an additional chest CT in which lung and MLNs (82 sites) were evaluated, and 21 patients had an additional head and neck CT in which neck LNs (21 sites) were evaluated. Therefore, a total of 1,060 sites were evaluated. Of these, 256 sites were recognized as positive by either FDG-PET or MRI-CT scan (score
Table 2  lists the details of false-positives and false-negatives in the FDG-PET scans. Granulation tissue or inflammatory change was the most common cause (four of six patients, 67%) for false-positives. In addition, radiation necrosis in the pelvic girdle and anthracosis in MLNs accounted for the other two false-positive results. Most commonly, false-negatives were in PLNs. After careful comparisons among clinical, pathologic, and PET data, seven (64%) of those with a false-negative result in the PLNs or primary, persistent, or recurrent local tumor (n = 11) had previous local pelvic RT. Two false-negatives might be metastatic lesions (2 and 5 mm, respectively), which are too small for FDG-PET scan detection. Low glucose transporter-1 (Glut-1) expression was found in 18% (three of 17 patients) of false-negative results. Missed interpretation of metastatic lesions in the peritoneal cavity, interpreted as bowel activity, was found twice and one SLN was misinterpreted as muscle activity.
Among the 94 patients with the 3-hour FDG-PET scan, 564 sites were compared between two PET protocols. Table 3 lists the detailed comparisons. There was recognition of 167 lesions (148 malignant, 19 benign) and 397 sites were considered true-negative, after both FDG-PET and MRI-CT were negative, with a negative follow-up for at least 6 months. Among the 148 documented malignant lesions, FDG-PET scans at 40 minutes only detected 116 (sensitivity, 79%; 95% CI, 71% to 85%). Eighteen additional lesions (sensitivity, 91%; 95% CI, 85% to 95%) were found in the 3-hour scans. These were in peritoneum (n = 3), bone (n = 1), PALNs (n = 4), PLNs (n = 7), and ILNs (n = 3; Figs 2 and 3). From the 416 benign sites evaluated (402 true-negative plus 14 false-positive results detected by 40-minute scans, or 412 true-negative plus four false-positive results detected by dual-phase scans), the false-positive rate was 3.4% for FDG-PET scans at 40 minutes. Ten (71%) of 14 patients with false-positive results by 40-minute scans were judged to be benign in subsequent 3-hour scans and so proven. Thus, the false-positive rate (for dual-phase scans) comprised 1% (four of 416) of results. These 10 sites were in peritoneum (n = 4), bone (n = 1), PALNs (n = 1), PLNs (n = 2), and ILNs (n = 2).
Sensitivity and specificity of FDG-PET scans at 40 minutes and using dual-phase scans were identical for primary, residual, and recurrent local tumors. For metastatic lesions in peritoneum, bones, PALNs, PLNs, and ILNs (n = 91), scans at 40 minutes detected 64 lesions (sensitivity, 70%; 95% CI, 60% to 80%) and dual-phase scans detected 82 lesions (sensitivity, 90%; 95% CI, 82% to 95%). The positive-predictive value and negative-predictive value of scans at 40 minutes only and dual-phase scans for primary, residual, and locally recurrent tumors were the same, whereas for metastatic sites, the positive-predictive value and negative-predictive value of scans at 40 minutes only were 82% (95% CI, 72% to 90%) and 93% (95% CI, 90% to 95%), respectively. For dual-phase FDG-PET scans, these two quantities became 95% (95% CI, 89% to 99%) and 98% (95% CI, 96% to 99%; Table 3  ), respectively. The ROC curve and AUC showed that the dual-phase FDG-PET scans were significantly superior to the 40-minute scans alone for metastatic lesions (P = .007; Fig 4). Dual-phase images alone were marginally better than 3-D early images (P = .052), and 3-D delayed images alone were marginally better than 2-D early images in metastatic lesions detection (P = .057).
The dual-phase scan results upstaged 25 patients (27%) and downstaged four patients (4%). With the additional information obtained, 23 patients (24%) had their treatment field and/or dosage changed and six patients (6%) then received palliative treatment.
MRI-CT studies have suboptimal accuracy because small or normally sized LN metastases may be missed (false-negative), whereas an enlarged reactive LN may produce a false-positive result.30 It is crucial to distinguish malignancy from benign inflammatory processes in previously treated regions. Unfortunately, MRI-CT scans have limitations in differentiating tumor infiltration from posttreatment inflammation, fibrosis, or scarring.2–5 PET, which gives functional images of FDG accumulation, could improve such discrimination. When false-negative PET scans were analyzed, three of six patients had small extrapelvic metastatic lesions ( 5 mm), whereas 64% of those with pelvic false-negatives had previous local pelvic RT. Low Glut-1 expression, misinterpretation of metastatic lesions as bowel activity, and a positive SLN misinterpreted as muscle activity accounted for the remaining false-negative patients after PET. The dual-phase FDG-PET protocol of this study was performed with a 2-D mode acquisition (40 to 96 minutes after injection) and a 3-D mode acquisition (180 to 210 minutes after injection). We chose the 3-D mode because it might allow higher sensitivity as a result of low count rates after the approximate 1.5-fold half-life of the tracer. In 3-D mode, the increased sensitivity to true events is partially offset by the coincident increased sensitivity to scatter and random events.21 Although the overall advantage of 2-D versus 3-D imaging is yet to be determined, in this study, we found that dual-phase images alone were marginally better than 3-D early images, and 3-D delayed images alone were marginally better than 2-D early images in the detection of metastatic lesions. Therefore, we advocate a combined analysis of early and late images. Because dual-phase FDG-PET scan was significantly superior to 40-minute scans for metastatic lesion detection, it allowed better salvage treatment planning, especially after RT and/or chemoradiotherapy, or equivocal FDG-PET results at 40 minutes. To the best of our knowledge,7–13,31,32 this is the first report of FDG-PET with dual-time scans in cervical cancer. Our LN detection rates (especially PLNs) exceed those of Williams’ series.13 In addition, the metastatic lesion detection accuracy in our cervical cancer patients after MRI-CT scans exceeded that quoted by others.31,33,34 After careful analysis, the sensitivity and specificity of MRI-CT scans for our patients 1 to 56 were similar to, but higher than, those for patients 57 to 135. This may be because MRI-CT scan diagnostic accuracy improved with time, after a learning curve from FDG-PET experience and pathologic or clinical follow-up results, or our patients had mainly locally advanced or recurrent or persistent cancers. Early cervical cancer patients were excluded because of the limited contributions expected from an FDG-PET scan. Thus, previously untreated cancers with small metastatic LNs (< 1 cm), which are easily missed by MRI-CT, were excluded from this study.
Our true-negative results are not totally satisfactory; at least two limitations are observed in FDG-PET scans. First, 6 months may be insufficient for follow-up of small ( Additional investigations of FDG uptake at the dual time points with enzyme expression (eg, Glut-1, hexokinase, and glucose-6-phosphatase)35–38 in cervical cancer are warranted. Hence, optimal schedules for FDG-PET scans to differentiate tumor cells from inflammation induced by RT and/or concurrent chemoradiotherapy could be determined for cervical cancer. Early detection of recurrence or more accurate initial staging or restaging on relapse does not automatically lead to improved long-term survival. The cost effectiveness of each indication has to be evaluated further in various clinical situations. On the basis of our preliminary data, several independent prospective trials are ongoing (using aspects of our selection criteria) for cervical carcinoma patients to be treated with curative intent. In conclusion, this study has confirmed that cervical cancer metastatic lesions are avid for FDG and that dual-phase FDG-PET is superior to conventional FDG-PET or MRI-CT for metastasis evaluation in locally advanced or recurrent cervical cancer. An additional delayed FDG-PET scan of the abdominal and pelvic regions provides supplementary useful information.
The authors indicated no potential conflicts of interest.
Supported by NSC 91-2314-B-182A-163 from the National Science Council Taiwan and CTRP 016 from the Chang Gung Memorial Hospital and University.
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Copyright © 2003 by the American Society of Clinical Oncology, Online ISSN: 1527-7755. Print ISSN: 0732-183X
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ABSTRACT
INTRODUCTION
; standardized uptake value, 2.89) was noted.
