OBJECTIVE. Accurate assessment of lymph node status before treatment is critical in the treatment of gynecologic cancers because the 5-year survival and ...
Detection of Pelvic Lymph Node Metastases in Gynecologic Malignancy: A Comparison of CT, MR Imaging, and Positron Emission Tomography A. D. Williams 1 C. Cousins 1 W. P. Soutter 2 M. Mubashar 1 A. M. Peters1 R. Dina 3 F. Fuchsel1 G. A. McIndoe 2 N. M. deSouza 1
OBJECTIVE. Accurate assessment of lymph node status before treatment is critical in the treatment of gynecologic cancers because the 5-year survival and treatment of women is influenced by lymph node involvement. The aims of this study were to investigate the ability of X-ray CT, MR imaging, and 18F-FDG positron emission tomography (PET) to detect pelvic lymph node metastases by comparing imaging with histopathologic findings after lymph node dissection. MATERIALS AND METHODS. Eighteen patients with gynecologic cancers were studied by all three imaging methods before surgery. The images were initially reviewed with routine diagnostic conditions and then, subsequently, by two observers who were unaware of the clinical and histopathologic findings of the patients. The nodal sites were split into upper (aortic to common iliac bifurcations) and lower (common iliac bifurcations to inguinal ligament) iliac chains. All observers’ results were statistically analyzed with specificity, sensitivity, positive and negative predictive values, Fisher’s exact test (individual observers) or chi-square test (combined observers), and Cohen’s kappa test. RESULTS. Eight of 18 patients had lymph node metastases at histology. Findings of all three modalities agreed in full in only one patient. CT correctly revealed 10 node-negative patients, whereas MR imaging was correct in eight of these patients. 18F-FDG PET correctly depicted one patient with lymph nodes negative for tumor. CT was the most specific imaging modality (97.0%), with MR imaging and PET rendering values of 90.7% and 77.3%, respectively, but sensitivity of all modalities was low (CT, 48.1%; MR imaging, 53.7%; PET, 24.5%). Observer agreement for each modality was good; kappa values among all observers were 0.88 for CT, 0.85 for MR imaging, and 0.72 for PET. CONCLUSION. CT is the most specific modality for detecting lymph nodes positive for tumor in gynecologic cancers, whereas MR imaging is the most sensitive. The poor results of PET in the pelvis are attributed to urinary 18F-FDG in the ureters or bladder, which may mask or imitate lymph node metastases.
Received November 27, 2000; accepted after revision February 2, 2001.
he choice of treatment in gynecologic malignancy is influenced by a physician’s prior knowledge of lymph node involvement with tumor. Lymph node metastases are also a vital prognostic factor; 5-year survival of women with node-positive tumors in cervical cancer varies between 42% and 67% [1, 2], compared with 87–92% for those with no detectable nodal metastases. Currently, baseline assessment of nodal involvement with tumor is undertaken with crosssectional imaging on CT or MR imaging, both of which rely on measurement of node size (long axis, short axis, or ratios of the two) [3, 4]. However, this assessment does not differentiate reactive enlargement of a node from malignant
Presented at the annual meeting of International Society for Magnetic Resonance in Medicine, Denver, April 2000. 1 Department of Imaging, Hammersmith Hospital, Imperial College School of Medicine, Du Cane Rd., London W12 0HS, United Kingdom. Address correspondence to A. D. Williams. 2 Department of Gynecological Oncology, Hammersmith Hospital, Imperial College School of Medicine, London W12 0HS, United Kingdom. 3 Department of Histopathology, Hammersmith Hospital, Imperial College School of Medicine, London W12 0HS, United Kingdom.
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infiltration. Positron emission tomography (PET) with 18F-FDG has been used as a functional method of determining tumor viability in several cancers including those of the head and neck [5–7], colon, and lung [8]. This method is based on increased glucose uptake that is associated with malignancy. The purpose of this study, therefore, was to compare cross-sectional (CT, MR) imaging with PET for the detection of pelvic nodal metastases in patients with gynecologic cancers. Materials and Methods Women with gynecologic cancers who underwent pelvic imaging on CT, MR imaging, and 18FFDG PET before pelvic lymph node excision were
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Williams et al. retrospectively analyzed. CT and MR imaging of the pelvis were performed as routine examinations in these patients, whereas PET was undertaken as a supplementary clinical investigation. Over a 2year period, 18 patients fulfilled these criteria: 16, cancer of the cervix: seven, squamous cell carcinoma; six, adenocarcinoma; two, adenosquamous cell carcinoma; and one, a rare Wilm’s tumor. Of the six patients with adenocarcinoma, two had recurrent disease. One patient had recurrence of endometrial cancer, and one had a vulval melanoma. The mean age of the women was 38.4 years (age range, 14–64 years). Imaging studies and subsequent surgery were performed over a 28-day period in 13 of 18 patients; in one patient, 61 days elapsed between initial imaging and surgery. CT Patients had bowel preparation with oral meglumine diatrizoate (Gastrografin; Schering Health Care, West Sussex, United Kingdom) (500 mL of a 2.5% solution) 2 hr before scanning. Images were obtained with Somatom Plus (eight patients) or Somatom Plus 4 (10 patients) scanners (Siemens, Erlangen, Germany). The patients were scanned from the symphysis pubis to the apex of the lungs, and all scans were contrast-enhanced with 100 mL of iopomide (Ultravist 300; Schering Health Care) [9]. In the Somatom Plus scanner, 10-mm contiguous slices were obtained for the pelvis and abdomen, and 10-mm reconstructed helical CT scans were obtained for the chest [10, 11]. Using the Plus 4 helical scanner, we obtained slices with 10-mm thickness image reconstruction in two acquisitions, pelvis to diaphragm and then chest. This procedure ensured that the liver was imaged in the portal phase. The initial images were reported by 11 radiologists (initial observer). MR Imaging Imaging was performed on a 0.5-T super-conducting magnet (Asset; Marconi Medical Systems, Highlands Heights, OH) with a pelvic phased array imaging coil. No prior patient preparation was used. At the start of scanning, each patient received 20 mg of intramuscular hyoscine-N-butylbromide (Buscopan; Boehringer-Ingelheim, Berks, United Kingdom) to reduce bowel motion artifact. The 35-cm field of view covered from the symphysis pubis to the bifurcation of the aorta. Coronal T1-weighted spinecho (TR/TE, 638/20), short tau inversion recovery fat-suppression sequences (2000/30; inversion time, 107 msec), sagittal T2-weighted fast spin-echo (TR/ effective TE, 4000/88), and transverse T1-weighted spin-echo (709/20) images with a slice thickness of 8 mm were obtained. Initially, the images were reviewed with routine clinical reporting conditions by one radiologist (initial observer) using an Alpha workstation (Digital Electronic Corporation, Houston, TX). PET PET whole-body images were obtained with an ECAT ART scanner (Siemens-CTI, Knoxville, TN) with a 16.2-cm axial field of view (reconstructed
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slice thickness, 10 mm; spatial resolution, 6 mm). The first five patients had no preparation, but the subsequent 13 fasted for at least 12 hr before the scan and had their blood glucose measured. None were excluded on the basis of hyperglycemia. The final 13 patients were well hydrated and given 20 mg of furosemide (Lasix; Borg Medicare, Herts, United Kingdom) intramuscularly to aid renal washout. Patients were injected with 88–222 MBq of 18F–FDG (mean, 165 MBq), and imaging was performed 37– 102 min after injection (mean, 55.6 ± 25.3 min). Patients emptied their bladders immediately before scanning. Studies were performed with a wholebody technique, mid thighs to ears, with a scan time of 45 min. Supine patients were scanned in 6–7 bed positions with 7 min in each position. Patients were scanned without initial transmission scans, so final images were not attenuation-corrected [12]. All images were displayed on a workstation monitor as three-dimensional black-and-white images. Two independent nuclear medicine physicians (initial observer) reviewed the studies initially with routine reporting conditions. Image Analysis Subsequently, independent observers, unaware of patient clinical and histopathologic details, assessed images formally for the purposes of this study. For each modality, an observer (first observer) with specialist experience in that particular modality and an observer (second observer) with a more general interest were used. Images were reviewed from either a soft or a hard copy, according to observer preference. Observers used prompt sheets specifying the nodal sites to ensure uniform responses. The nodal regions scored were divided into left and right and upper and lower iliac chain areas. The upper iliac lymph node chain extended from aortic to iliac bifurcations; the lower iliac node chains extended from the common iliac bifurcations to the inguinal ligaments. These divisions were chosen because they could be easily identified on PET scans and simplified the imaging analysis. The patients imaged were not consecutive. They were referred for PET scanning on the basis of large stage Ib cervical cancer, small tumors with parametrial extension, or recurrent pelvic disease. Imaging with PET was also dependent on staffing and radiopharmaceutical availability, because this was a new modality in the main imaging department. Nodal positivity was determined by size on MR imaging and CT; nodes greater than 1-cm long axis were noted as positive for tumor. Findings of focal 18F-FDG uptake along the iliac chains were noted as positive on PET. Histology At pelvic lymph node dissection, all tissues were labeled for site and side and documented by the senior operating room technician or assisting clinician. The surgical specimens were fixed in formalin. The lymph nodes were macroscopically described for size, form, and nature and then embedded in paraffin wax. They were bisected before embedding in paraffin, routinely processed, and stained with H and E
before microscopic examination. Any metastases identified were typed to ensure that they were from the primary tumor. Histology was obtained for every lymph node dissected, and all tumors were staged according to the international primary TNM classification [13]. The histologic slides were retrospectively reviewed in all patients. The maximal lengths of all available lymph nodes with positive and negative findings were recorded with a centimeter scale. Statistical Analysis Comparison with histology was made for right and left and upper and lower iliac regions for each imaging modality and for each observer. Thus, the number of true-positives, true-negatives, false-positives, and false-negatives for every patient in each of four nodal sites was tabulated. The sensitivity, specificity, and positive and negative predictive values were calculated with standard statistical formula. Cohen’s kappa tests [14] were applied to test observer agreement in each modality. Each observer’s results for both iliac sites and combined sites were subjected to a Fisher’s exact test, a 2 × 2 table with positive/negative findings on histology versus each reviewer’s observations. Chi-square tests, a 2 × 2 table with positive and negative findings on histology versus observers, were used for the combined results for all observers of each modality to test the hypothesis that the observers had not arrived at their agreement with histology by chance. A p value of 0.05 was chosen to indicate a 95% probability that the results were achieved by expert observation of the imaging modality.
Results
Findings in 10 patients were negative for metastatic lymph nodes, and in the remaining eight, malignant nodes were shown in the upper iliac region (one patient), lower iliac region (five patients), or in both (two patients). The number of true-positives, true-negatives, false-positives, and false-negatives for every patient in each of four nodal sites was tabulated. Table 1 shows the totals of these figures for each modality, as upper, lower, and combined results. Tables 2–4 give the sensitivity and specificity results for each radiologist and the combined results for all radiologists for each modality. Table 2 is for the upper, and Table 3 is for the lower iliac region. Sensitivity and specificity for upper and lower iliac sites were similar for each modality. Overall, CT achieved the highest specificity, 97.0%, whereas specificity with MR imaging was 90.7% and with PET, 77.3%. Although the sensitivity was poor on CT (48.1%) and MR imaging (53.7%), it was low for PET (24.5%) (Table 4). A patient with findings of true-positive nodes is illustrated in Figure 1. Examples of false-positive nodes are shown in Figures 2 and 3.
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TABLE 1
Imaging of Pelvic Lymph Node Metastases
Combined Observers’ Results for All Modalities Compared with Histology
Modality (Combined Observers)
True-Positive
False-Positive
True-Negative
False-Negative
8 17 25
2 3 5
91 68 159
7 20 27
8 21 29
7 8 15
86 61 147
7 8 15
4 9 13
16 21 37
77 49 126
11 29 40
CT Upper nodes Lower nodes All nodes MR imaging Upper nodes Lower nodes All nodes PET Upper nodes Lower nodes All nodes
Note.—PET = positron emission tomography.
TABLE 2
Sensitivity and Specificity of All Modalities for the Upper Iliac Region
Observer Test Initial observera First observer b Second observer c All observers
CT
MR Imaging
PET
Sensitivity (%)
Specificity (%)
Sensitivity (%)
Specificity (%)
Sensitivity (%)
Specificity (%)
40 40 80 53.3
100 100 93.5 97.9
60 40 60 53.3
93.6 93.6 90.3 92.5
20 40 20 26.7
93.6 87.1 67.7 82.8
Note.—PET = positron emission tomography. a Reporting clinician at the time of the scan. b Experienced radiologist with specialist interest who interpreted the images unaware of all clinical information. c Experienced radiologist with a more general interest who interpreted the images unaware of all clinical information.
TABLE 3
Sensitivity and Specificity of All Modalities for the Lower Iliac Region
Observer Test Initial observera First observer b Second observer c All observers
CT
MR Imaging
PET
Sensitivity (%)
Specificity (%)
Sensitivity (%)
Specificity (%)
Sensitivity (%)
Specificity (%)
38.5 58.3 41.7 46.0
100 95.8 91.7 95.8
53.9 61.5 46.2 53.9
91.3 78.3 95.7 88.4
30.8 23.1 16.7 23.7
73.9 47.8 87.5 70.0
Note.—PET = positron emission tomography a Reporting clinician at the time of the scan. b Experienced radiologist with specialist interest who interpreted the images unaware of all clinical information. c Experienced radiologist with a more general interest who interpreted the images unaware of all clinical information.
TABLE 4
Positive and negative predictive values are given in Table 5. The results for each modality were similar for upper and lower iliac sites. For both iliac sites combined, CT had the highest positive predictive value (0.83) and a negative predictive value equal to MR imaging (0.85), whereas PET had the lowest positive predictive value (0.26), because of the high number of false-positive findings. Observer Agreement
The results of Cohen’s kappa tests of agreement among all radiologists for each modality are given in Table 6. For CT, the agreement among all observers for upper and lower iliac node sites combined was good, with kappa values for observer combinations varying between 0.85 and 0.94. CT had the highest agreement among all observers (κ = 0.88). For MR imaging, kappa values were also high (0.81–0.87). Agreements among observers for the nodal sites combined in PET were good, albeit slightly lower (κ = 0.64–0.79). The Fisher’s exact test indicated that it was unlikely that any CT observers would have reached their agreement with histology by chance, because all observers had probability scores of less than 0.05. With MR imaging, the Fisher’s exact test also indicated that observers were unlikely to have arrived at their results by chance ( p < 0.05). For PET, the results of Fisher’s exact test for upper and lower iliac sites separately and for the iliac sites combined was more than 0.05, indicating a greater than 5% probability that all observers could have arrived at their results by chance.
Agreement Among Modalities
Findings on all three modalities agreed on all sites in only one node-negative patient. CT correctly reported all 10 node-negative patients, whereas findings on MR imaging agreed in eight of these. 18F-FDG PET correctly showed one patient with a true-negative lymph node status.
Sensitivity and Specificity of Modalities for Both Iliac Regions Histologic Analysis
Observer Test Initial observer a First observer b Second observer c All observers
CT
MR Imaging
PET
Sensitivity (%)
Specificity (%)
Sensitivity (%)
Specificity (%)
Sensitivity (%)
Specificity (%)
38.9 52.9 46.7 48.1
100.0 98.2 94.7 97.0
55.6 55.6 50.0 53.7
92.6 87.0 92.6 90.7
27.8 27.8 17.7 24.5
85.2 70.4 76.4 77.3
Note.—PET = positron emission tomography. a Reporting clinician at the time of the scan. b Experienced radiologist with specialist interest who interpreted the images unaware of all clinical information. c Experienced radiologist with a more general interest who interpreted the images unaware of all clinical information.
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Five hundred and four lymph nodes were resected and documented. Macroscopiclength measurements in 33 of 34 nodes containing metastatic deposits were obtained (Fig. 4). The mean length of positive nodes was 1.1 ± 0.6 cm (median, 0.9 cm; range, 0.2– 2.3 cm). Of the nodes recorded as positive for tumor, 54.5% were less than 1.0 cm in length (45.5% ≥ 1.0 cm in length). Four hundred seventy nodes were negative for tumor, and it was possible to obtain length measurements in 314
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Williams et al. Fig. 1.—33-year-old woman with endometrial cancer and histologically confirmed lymph node metastases. A, Transverse CT scan through pelvis shows enlarged lymph node (arrow ) in right iliac region above level of common iliac bifurcation. B, Coronal spin-echo T1-weighted MR image (TR/TE, 720/20) shows bilateral enlarged lymph nodes (arrows ). C, Coronal positron emission tomography scan shows foci of increased uptake in both iliac chains (black arrow ) and in left supraclavicular region (white arrow ).
A
A
B
B
Fig. 2.—26-year-old woman with clinical stage I cervical cancer and histology negative for tumor. A, Coronal spin-echo T1-weighted MR image (TR/TE, 720/20) through mid pelvis shows enlarged lower iliac node on right (arrow). B, Coronal short tau inversion recovery MR image (TR/TE, 2500/30; inversion time, 107 msec) through mid pelvis, at same level as A, shows enlarged lower iliac node on right (arrow ).
of these. The mean length of negative nodes was 0.7 ± 0.5 cm (median, 0.6-cm; range, 0.1–2.5 cm). Of the nodes negative for tumor, 22.6% were equal to or greater than 1.0 cm in length (77.4% > 1.0 cm in length). The difference in the length of positive and negative lymph nodes recorded on macroscopy was significant ( p = 0.0).
Discussion
This study emphasizes the difficulties of detecting lymph nodes involved with tumor in the pelvis with cross-sectional imaging and PET. The problems encountered with cross-sectional imaging modalities have led to repeated investigation of the criteria by which such nodes are
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identified to improve the sensitivity of detection [15–17]. The intrinsic problem has always been separating normal-sized nodes with tumor deposits from nodes that may be reactively enlarged. Traditionally, a single long-axis measurement of the node is used, but lately, both long- and short-axes measurements and even ratios have been tried [4]. Some systems take into account nodal shape with round nodes scoring higher for malignant involvement than ovoid or elongated ones [18]. With the advent of newer imaging modalities such as MR imaging and PET, it was hoped that other criteria such as the signal intensity [17] of the node or its metabolic status [5–7] might prove a more sensitive indicator of disease. However, preliminary results have
C
Fig. 3.—Coronal positron emission tomography scan of 42-year-old woman with cervical cancer shows focus of increased uptake in left lower iliac region (arrow ). Histology of lymph nodes was negative for tumor.
been disappointing, and morphologic criteria alone are used. Further refinements include contrast enhancement [18, 19] and studies of oxygenation of the node [20], but even in a research setting, these parameters remain unreliable. This study, therefore, used size criteria alone to detect lymph nodes positive for tumor with respect to CT and MR imaging. As in others, this study also used a 1-cm-long axis cutoff [5, 16]. A lower figure would reduce the specificity, particularly in the pelvis where adjacent bowel creates difficulties with partial volume effects. The positive predictive value of CT was higher than that of the other two modalities. CT was, thus, of intermediate sensitivity, but highly specific. On MR imaging, observers obtained
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Imaging of Pelvic Lymph Node Metastases
TABLE 5
Positive and Negative Predictive Values for Each Modality
Site
Positive Negative Modality Predictive Predictive Value Value
Upper iliac
Lower iliac
Combined iliac
CT MR imaging PET
0.80 0.53
0.93 0.92
0.20
0.88
CT MR imaging PET
0.85 0.72
0.77 0.77
0.30
0.63
CT MR imaging PET
0.83 0.66
0.85 0.85
0.26
0.76
Note.—PET = positron emission tomography.
equal or slightly higher sensitivity ratings than on CT, because contrast between tissues was better on T2-weighted MR sequences. However, specificity was slightly lower. The positive predictive values for MR imaging were, therefore, low, because both observers had a number of false-positive findings. Low sensitivity and specificity results were obtained overall for PET imaging. These results were disappointing, because PET has become more widely used for staging of head and neck cancers, in lung cancer, and in malignant melanoma [5–8, 21]. This study emphasized the many problems facing 18F-FDG PET in the pelvis [22]. Residues of 18F-FDG can
Fig. 4.—Photomicrograph of microscopic deposit in lymph node (arrow ) of 62-year-old woman with cervical cancer shows overall length to be 14.5 cm. (H and E, ×5)
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TABLE 6
Agreement Between Observers for Each Imaging Modality for Combined Iliac Sites
Modality
CT MR imaging PET
κ (Initial and First Observers)
κ (First and Second Observers)
κ (Initial and Second Observers)
κ (All Observers)
0.94 0.87 0.79
0.85 0.81 0.64
0.86 0.87 0.73
0.88 0.85 0.72
Note.—Initial observer = reporting clinician at the time of the scan, first observer = experienced radiologist with specialist interest who read the images unaware of all clinical information, second observer = experienced radiologist with a more general interest who read the images unaware of all clinical information, PET = positron emission tomography.
sometimes be seen in the ureters and in the bladder, masking or imitating metastases. These technical problems must be addressed to improve the specificity of the technique [23]. The requirement for histologic correlation after node dissection introduced bias into the study. Patients with unequivocally enlarged nodes would not have undergone surgical lymph node dissection but would have been selected for radiation therapy and would, therefore, have been excluded from analysis. Also, patients with small primary tumors and nodes not enlarged on initial investigation with crosssectional imaging may not have been referred routinely for PET scanning. The population selected will, thus, have been patients destined for surgical lymph node dissection with a likelihood of small lymph node metastases. Observer bias was minimized by using a uniform prompt sheet and by ensuring the first and second observers were unaware of the clinical and histopathologic details. CT is a well-estab-
Fig. 5.—Photomicrograph of lymph node in 33year-old woman with endometrial cancer shows node largely replaced by tumor. Overall length is 8.0 cm. (H and E, ×5)
lished imaging modality, and as expected, the overall agreement among radiologists reviewing CT was high. In view of the good agreement among multiple observers, it can be concluded that the shortcomings of this modality are due to the choice of criteria for detection of the lymph nodes positive for tumor and technical factors rather than to observers’ abilities. MR imaging is also routinely used for pelvic imaging, and, as with CT, the agreement among radiologists reviewing this modality was good. With PET, observers agreed on 11 patients for both the upper and lower iliac regions. This was good agreement in the modality, but only four agreed observations were correct compared with histology. There were no truepositive reports on which all three observers agreed. The use of PET in the pelvis is a relatively new phenomenon [24], and the poor results may be attributed partly to lack of observer experience. CT has the advantages of better total-body coverage and short scanning time. Radiation dose is not an issue in this group of patients. The limitations of MR imaging are long scanning times and poor total-body coverage, but it offers superior definition of the primary disease. PET performs poorly in the pelvis because of inherent problems of imaging the pelvis with 18FFDG. These problems currently are being addressed with further improvements in patient preparation. A combination of morphologic and functional techniques or multitracer PET studies may improve sensitivity further. Cross-sectional imaging modalities are only moderately sensitive for detection of lymph node metastases in the pelvis, based on size criteria. However, a functional technique with a glucose analogue (18F-FDG) PET also performs poorly because of radioactive residues in the ureters and bladder. Acknowledgments
We thank Daphne Glass for her invaluable help with the PET studies, Jayne Morgan for help with
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Williams et al. CT, T. Krausz for his help with the histologic analysis, and B. Puri for his statistical advice. We are grateful to Mary Crisp for her secretarial assistance.
8.
References 1. Tanaka Y, Sawada S, Murata T. Relationship between lymph node metastases and prognosis in patients irradiated postoperatively for carcinoma of the uterine cervix. Acta Radiol Oncol 1984;23:455–459 2. Anderson MC, Coulter CAE, Mason WP, Soutter WP. Malignant disease of the cervix. In: Shaw RW, Soutter WP, Stanton Sl, eds. Gynecology, 2nd Ed. New York: Churchill Livingstone, 1997:541–568 3. Carrington B. Lymph Nodes. In: Husband JES, Reznek RH, eds. Imaging in oncology, Oxford, England: ISIS Medical Media, 1998:729–748 4. Steinkamp HJ, Cornehl M, Hosten N, Pegios W, Vogl T, Felix R. Cervical lymphadenopathy: ratio of long- to short-axis diameter as a predictor of malignancy. Br J Radiol 1995;68:266–270 5. Adams S, Baum RP, Stuckensen T, Bitter K, Hor G. Prospective comparison of 18F-FDG PET with conventional imaging modalities (CT, MR imaging, US) in lymph node staging of head and neck cancer. Eur J Nucl Med 1998;25:1255–1260 6. Braams JW, Pruim J, Freling NJ, et al. Detection of lymph node metastases of squamous-cell cancer of the head and neck with FDG-PET and MR imaging. J Nucl Med 1995;36:211–216 7. Laubenbacher C, Saumweber D, Wagner-Manslau C, et al. Comparison of fluorine-18-fluorode-
348
9.
10.
11.
12. 13. 14. 15.
16.
oxyglucose PET, MR imaging and endoscopy for staging head and neck squamous-cell carcinomas. J Nucl Med 1995;36:1747–1757 Steinert HC, Hauser M, Allemann F, et al. Nonsmall cell lung cancer: nodal staging with FDG PET versus CT with correlative lymph node mapping and sampling. Radiology 1997;202:441–446 Gocke P, Gocke C, Neuman K, Henseke P, Langer R, Muller RD. Prospective randomized study for an injection protocol for intravenous contrast media in abdominal and pelvic helical CT. Acta Radiol 1999;40:515–520 Fukuda H, Nakagawa T, Shibuya H. Metastases to pelvic lymph node from carcinoma in the pelvic cavity: diagnosis using thin-section CT. Clin Radiol 1999;54:237–242 Naik KS, Spencer JA, Craven CM, MacLennan KA, Robinson PJ. Staging lymphoma with CT: comparison of contiguous and alternate 10-mm slice techniques. Clin Radiol 1998;53:523–527 Bailey DL. Transmission scanning in emission tomography. Eur J Nucl Med 1998;25:774–787 Sobin L, Wittekind C. TNM Classification of malignant tumors. New York: Wiley, 1997:131–164 Cohen J. A coefficient of agreement for nominal scales. Educ Psych Meas 1960;20:37–46 Matsukuma K, Tsukamoto N, Matsuyama T, Ono M, Nakano H. Preoperative CT study of lymph nodes in cervical cancer: its correlation with histological findings. Gynecol Oncol 1989;33:168–171 Kim SH, Choi BI, Han JK. Preoperative staging of uterine cervical carcinoma: comparison of CT and MR imaging in 99 patients. J Comput Assist
Tomogr 1993;17:633–640 17. Kim SH, Kim SC, Choi BI, Han MC. Uterine cervical carcinoma: evaluation of pelvic lymph node metastasis with MR imaging. Radiology 1994;190:807–811 18. Kvistad KA, Rydland J, Smethurst HB, Lundgren S, Fjosne HE, Haraldseth O. Axillary lymph node metastases in breast cancer: pre-operative detection with dynamic contrast-enhanced MR imaging. Eur Radiol 2000;10:1464–1471 19. Yang WT, Lam WW, Yu MY, Cheung TH, Metreweli C. Comparison of dynamic helical CT and dynamic MR imaging in the evaluation of pelvic lymph nodes in cervical carcinoma. AJR 2000;175:759–766 20. Robinson SP, Collinridge DR, Howe FA, Rodrigues LM, Chaplin DJ, Griffiths JR. Tumor response to hypercapnia and hyperoxia monitored by FLOOD magnetic resonance imaging. NMR Biomed 1999;12:98–106 21. Gritters LS, Francis IR, Zasadny KR, Wahl RL. Initial assessment of positron emission tomography using 2-fluorine-18-fluoro-2-deoxy-D-glucose in the imaging of malignant melanoma. J Nucl Med 1993;34:1420–1427 22. Strauss LG. Fluorine-18 deoxyglucose and false-positive results: a major problem in the diagnostics of oncological patients. Eur J Nucl Med 1996;23: 1409–1415 23. Moran JK, Lee HB, Blaufox MD. Optimization of urinary FDG excretion during PET Imaging. J Nucl Med 1999;40:1352–1357 24. Heicappell R, Muller-Mattheis V, Reinhardt M, et al. Staging of pelvic lymph nodes in neoplasms of the bladder and prostate by positron emission tomography with 2-[(18)F]-2-deoxy-D-glucose. Eur Urol 1999;36:582–587
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