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1 All authors: Department of Radiology, University of Rome "La Sapienza," V.le Regina Elena 324, 00161 Rome, Italy.
Received May 13, 2002;
accepted after revision October 22, 2002.
Address correspondence to C. Catalano.
Abstract
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MATERIALS AND METHODS. Forty patients with suspected renal cell carcinoma underwent MDCT. Contrast-enhanced acquisitions were obtained during arterial, nephrographic, and urographic phases using a thin-slice protocol. One-millimeter-thick source images were evaluated by two observers on a dedicated workstation for the identification and characterization of the tumor, presence of a pseudocapsule or invasion of perirenal fat, involvement of adrenal glands or surrounding tissues, presence of satellite lesions within Gerota's fascia, infiltration of renal vein and inferior vena cava, involvement of lymph nodes, and presence of distant metastases. Imaging findings were compared with surgical specimens using criteria from the Robson and TNM classification systems.
RESULTS. The presence and size of all lesions were correctly shown in all patients. In evaluating Robson stage I of renal cell carcinoma, we were able to diagnose fat infiltration on 1-mm scans with 96% sensitivity, 93% specificity, and 95% accuracy; the positive and negative predictive values were, respectively, 100% and 93%. One hundred percent accuracy was achieved in staging high-grade lesions.
CONCLUSION. High-resolution MDCT is accurate in the preoperative evaluation of patients with renal cell carcinoma.
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Progress in surgical techniques has shown that conservative surgery, even laparoscopic, can be successfully used in patients with small capsulated lesions (Robson stage I [2]), in patients with carcinoma in a solitary functioning kidney, in patients with compromised renal function, and in patients with multiple bilateral tumors [2, 3, 4, 5, 6]. Before conservative surgery is performed to spare as much normal parenchyma as possible, an accurate preoperative imaging study is required to acquire all the needed anatomic information concerning the renal parenchyma and the vascular and collecting system structures and to stage the neoplasm [7, 8].
The recent introduction of multidetector CT (MDCT) into clinical practice has allowed radiologists to overcome most of the limitations of single-detector helical CT. In particular, the very thin-slice collimation, the high speed of acquisition, and the near isotropy of the voxels allow the reformatting of images in any plane without significant artifacts and with excellent anatomic detail [9, 10, 11, 12]. The high spatial resolution obtained with high-resolution protocols makes this technique particularly suitable for the assessment of most vascular and abdominal abnormalities [2, 13, 14, 15] and for the evaluation of renal neoplasms.
The purpose of our study was to evaluate the accuracy of MDCT using a high-resolution protocol and a real-time interaction approach with the three-dimensional (3D) data set for image evaluation with the aim of providing all anatomic and pathologic information necessary to correctly stage and to adequately plan treatment.
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Examination Technique
Helical CT was performed using an MDCT scanner (Volume Zoom; Siemens,
Forcheim, Germany) with a gantry rotation of 0.5 sec. In all patients, four
phases were acquired: an unenhanced scan from the thorax to the kidneys to
identify lung metastases, renal calcifications, and intratumoral fat; an
arterial phase to evaluate the renal cortex, renal arteries, and tumoral
vascularization; a parenchymal phase, which was more sensitive than the other
phases, to detect small lesions and to assess renal venous drainage; and an
excretory delayed phase to evaluate the relationship between the tumor and the
collecting system. The arterial and parenchymal phase scans were acquired in a
craniocaudal direction from the diaphragm to the lower pole of the kidneys,
whereas the excretory phase scans were acquired from the upper pole of the
kidneys to the bladder.
Unenhanced scanning was performed using the following parameters: collimation, 4.0 x 2.5 mm; slice thickness, 5 mm; reconstruction interval, 5 mm; table feed, 12 mm/rotation; 130 mAs; and 120 kVp. Contrast-enhanced scanning was performed using the following parameters: collimation, 4 x 1 mm; slice thickness, 1.25 mm; reconstruction interval, 1 mm; table feed, 5 mm/rotation; 160 mAs; and 120 kVp.
All patients received an injection of a standard dose of 140 mL of iomeprol 350 (Iomeron 350; Bracco, Milan, Italy) through an 18-gauge peripheral venous access (generally an antecubital vein) at a flow rate of 4 mL/sec; the start delay was 22 sec for the arterial phase and 50–60 sec for the parenchymal venous phase. The excretory phase was acquired 5 min after the start of the injection. The bolus injection technique was used to administer contrast material with an automated injector (En-Vision CT; Medrad, Indianola, PA) and was carefully monitored by a physician. All patients underwent scanning in the supine position.
One-millimeter-thick CT images were analyzed using a real-time interaction approach on a dedicated workstation (Kayak XU 800; Hewlett-Packard, Palo Alto, CA) with 3D rendering software (Vitrea 2.6; Vital Images, Plymouth, MN). The mean duration time was 30 min including real-time interaction on the 3D workstation.
Image Reconstruction
One-millimeter-thick data sets were postprocessed using different
algorithms. Selective thin (10–50 mm) maximum intensity projections were
performed for evaluation of arterial and venous vascular anatomy and for
assessment of the collecting system in the excretory phase. Multiplanar
reformatted images were obtained from all data sets to evaluate the neoplasm
and its relationship with normal parenchyma and to acquire information on
venous anatomy and drainage. In some cases, reconstructions using a
volume-rendering algorithm were also performed.
Image Evaluation
Axial and reformatted images were evaluated by two radiologists who were
unaware of the results, with the final diagnosis reached by consensus. CT
images were evaluated to obtain parenchymal and vascular anatomy information
(number of main renal arteries, veins, and supernumerary vessels).
Tumor staging included the following parameters: identification and characterization of the tumor (localization and extension), presence of a pseudocapsule (a thin band of fibrous tissue and compressed renal parenchyma surrounding the lesion) or invasion of perirenal fat (determined by the presence of small hyperdense streaks and nodules surrounding the lesion), involvement of adrenal glands or surrounding tissues, presence of satellite lesions within Gerota's fascia, evaluation of renal vein and inferior vena cava, involvement of lymph nodes, and presence of distant metastases. All the parameters were evaluated to determine the stage of the disease according to criteria based on either the Robson or the TNM classification system [16] (Appendix 1).
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The results of the interpretations were entered in a database (Excel for
Office 2000; Microsoft, Redmond, WA) and were evaluated for strength of
agreement using the Cohen kappa statistics (SPSS 8.0 for Windows; SPSS,
Chicago, IL) to determine poor (
< 0), slight ( =
0.01–0.20), fair ( = 0.21–0.40), moderate ( =
0.41–0.60), substantial ( = 0.61–0.80) and almost perfect
( = 0.81–1.00) agreement beyond that of chance alone. Imaging
findings were compared with operative findings, gross specimens, and
pathologic diagnosis in all patients.
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A pseudocapsule was present in 16 patients who were candidates for nephron-sparing surgery; in one of these patients, perinephric fat tissue infiltration was shown at surgery, and the laparoscopic approach had to be converted into open surgery.
Adrenal glands were involved in nine patients. Renal vein or inferior vena cava thrombosis was detected in 12 patients. Lymph node involvement with adenopathies larger than 1 cm in diameter was found in 14 patients; pathologic examination showed metastatic disease in 13 patients and nodal reactive hyperplasia in one patient. Distant metastases were seen in six patients, with multiple lung metastases in two patients confirmed at follow-up; and 14 liver metastases were detected on intraoperative sonography in the other four patients.
Vascular anomalies were found in seven patients: one patient with triple renal artery; four with double renal artery, one of whom also presented with a double renal vein; one with retroaortic left renal vein; and one with left circumaortic renal vein.
Surgical findings proved that 15 patients were Robson stage I, four were Robson stage II, five were Robson stage IIIa, three were Robson stage IIIb, three were Robson stage IIIc, four were Robson stage IVa, and six were Robson stage IVb.
MDCT Findings
Results of MDCT findings are shown in
Figure 1. The presence and size
of all lesions were correctly shown in all patients, including those patients
with bilateral neoplasm and two lesions in the same kidney (Figs.
2A,
2B and
2C).
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In 16 patients, tumor was considered confined by a pseudocapsule, with no evidence of perinephric spread in 15 of them (Figs. 3A, 3B and 3C). In one patient, thickening of perirenal fat was present but was associated with a previous inflammation, as mentioned in the patient's clinical history, and for this reason, the tumor was equally considered to be Robson stage I.
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Correct assessment of infiltration of caliceal infiltration was also achieved in all patients (Figs. 4A, 4B).
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In those patients with renal vein or inferior vena cava thrombosis, MDCT was able to correctly identify and localize the extent of the thrombus in all patients (Figs. 5A, 5B and 5C). Distant metastases were correctly seen in six patients: two patients had multiple pulmonary nodules and four patients had liver lesions.
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In the evaluation of liver metastases, MDCT detected the presence of all 14 lesions, with three identified only in the arterial phase, seven in the portal venous phase, and four in both phases.
With regard to lymph node involvement, 18 adenopathies were identified; of these, 14 were larger than 1 cm. Those that were round were classified as malignant, whereas the others were classified as reactive hyperplasia.
Multiplanar reformatted images and thin maximum-intensity-projection images correctly showed all vascular anomalies, either arterial or venous (Fig. 2C).
Consensus interpretation of 1-mm axial scans and real-time interaction showed that 16 patients were classified as Robson stage I, three were Robson stage II, five were Robson stage IIIa, three were Robson stage IIIb, three were Robson stage IIIc, four were Robson stage IVa, and six were Robson stage IVb.
Analysis of interobserver variability showed an almost perfect (
> 0.81) agreement. The observers disagreed in two patients. One patient who
presented with minimal perirenal fat infiltration was correctly classified by
one radiologist as Robson stage II and as Robson stage I by the other
radiologist. Another patient, defined at surgery as Robson stage IIIa because
of renal vein thrombosis, was correctly classified by one radiologist as
Robson stage IIIa and as Robson stage IIIc by the other radiologist, who
defined a centimetric hyperplastic lymph node as metastatic.
In evaluating stage I of renal cell carcinoma for fat infiltration, the observers were able to reach a diagnosis on 1-mm scans with 96% sensitivity, 93% specificity, and 95% accuracy; the positive and negative predictive values were, respectively, 100% and 93%.
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Helical CT, although well established and widely accepted as the preferred imaging technique in patients with renal cell carcinoma, still has some limitations, mainly concerning the difficulty in differentiating Robson stage I from II. The presence of pseudocapsule or its infiltration by a significant amount of tumoral tissue is a specific sign, which, nevertheless, cannot always and easily be recognized [8, 17, 18]. With the recent surgical developments, this sign represents in some centers the main limitation for a conservative, possibly laparoscopic approach, which is feasible in Robson stage I when no evidence of perinephric fat invasion is present [19, 20].
Multidetector technology is the most recent development in helical CT that has allowed improvement in the diagnostic accuracy of CT in several anatomic areas because of the use of thin collimation and the ability to reveal data not only in the axial plane but also with multiplanar reformatting. Involvement of perirenal fat tissue represents a key point in treatment planning. In fact, the infiltration of perirenal fat tissue modifies the surgical approach from conservative to radical nephrectomy [21, 22, 23, 24, 25]. In this group of patients, 15 lesions appeared well capsulated and were correctly defined on MDCT by both observers as Robson stage I. In one patient, whose lesion was defined on MDCT as Robson stage I, the lesion turned out to be stage II at surgery because of involvement of perirenal fat tissue, and the surgical approach had to be converted into a laparotomy. A retrospective analysis showed that the probable cause of the misinterpretation was the presence of perinephric edema that was erroneously related to previous inflammatory processes (Figs. 6A, 6B). Perinephric spread of tumor has been reported as the most common cause of under- and overstaging of renal cell carcinoma on CT [8]. In this study, although the number of patients was limited, only one case of understaging occurred, and there were no false-positive findings. The use of a high-resolution protocol during the vascular phases allowed us to better detect small enhancing nodules as typical features of perinephric involvement and to assess edema and venous engorgement as benign causes of perirenal stranding.
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The diagnosis of malignancy with regard to lymph node involvement is still based on size criteria only. With 10 mm as the limiting size for normal nodes, 4% of lymph nodes have a false-negative finding because micrometastases cannot be identified. Furthermore, false-positive findings can be between 3% and 43%, according to different studies [26, 27], because nodal enlargement may be determined by reactive hyperplasia [26]. The reported accuracy of conventional CT in lymph node involvement is between 83% and 88% [27]. Although a limited number of patients with metastatic adenopathy were present in our group, MDCT allowed us to identify all cases of adenopathy, even those smaller than 10 mm. Nevertheless, it has been recently shown that there is no clinical benefit in performing regional lymph node dissection in patients with no suspected adenopathy before surgery or in those patients with lymph nodes smaller than 10 mm [28].
The evaluation of renal vein and inferior vena cava thrombosis is crucial for treatment planning; in fact, if tumor thrombus spreads into the inferior vena cava, the exact extent of the thrombus is essential for planning the correct surgical approach: an abdominal incision is performed if the thrombus is infrahepatic, whereas a thoracoabdominal incision is needed if the thrombus extends more cranially. The high-resolution protocol, which allows high-quality multiplanar reformatting, provides detailed anatomic information essential for a correct diagnosis and provides a more familiar orientation for surgeons. Although in our series the number of patients with renal vein or inferior vena cava thrombosis was limited, 3D real-time interaction allowed the correct identification of both in all patients.
Staging of renal cell carcinoma also requires assessment of the lungs and liver where metastases can be found. Metastatic lesions to the liver may be, like the primary tumor, hypervascular [2]; it is therefore necessary to examine the liver not only in the portal venous phase but also in the arterial phase. Although the prognosis of patients with liver metastases is poor, patients with a single hepatic lesion may benefit from metastasectomy [29]. Even with a high-resolution protocol, it is possible with MDCT to examine the entire upper abdomen in either the arterial phase or the portal venous phase.
MDCT allowed us to correctly detect all cases of adrenal infiltration. The current surgical trend is to spare adrenal glands that appear normal on CT, which is also based on a previous study that showed a 100% negative predictive value for spread of tumor to the adrenal glands [30]. Adrenal glands and their relationship to the tumor are better shown on multiplanar and, particularly, coronal reformatted images.
In correctly staging renal cell carcinoma, we found that the advantages of multiplanar images were evident, as shown in our study and as shown by several MR imaging studies [31, 32]. Single-detector helical CT allowed axial images to be reformatted into coronal, sagittal, or oblique planes, but the reconstructions were limited in quality, especially because of anisotropy.
Previous helical CT studies using a standard protocol showed a limited accuracy of the technique in the determination of tumor spread in the perinephric space [8, 18].
Moreover, other authors [33] have recently noted that, in some cases, accessory renal arteries and veins can be missed using a standard helical CT protocol and that although 3D CT decreased the dependence on intraoperative sonography, it did not eliminate it, particularly in better localizing the intrarenal extent of the tumor.
In our study, high-resolution MDCT allowed the depiction of accessory renal arteries and veins in all patients, as well as the renal extent of the tumor.
Several studies have shown that narrow collimation (4 x 1 mm) effectively reduces partial volume effects and corresponding artifacts with significant improvement of image quality [34, 35]. The ability of dual-phase CT of the kidney to provide parenchymal and vascular information has already been well documented [8]; the use of the excretory phase improves determination of the intrarenal extent of the tumor and the relationship with the collecting system.
A limitation of such a high-resolution protocol is represented by the radiation dose to the patient (weighted-CT dose index: 18.81 mGy using 4 x 1 mm collimation; 15.49 mGy using 4.0 x 2.5 mm collimation [36]). Accordingly, the radiology community is well aware of the additional radiation burden brought by high-resolution MDCT protocols.
Detailed information on renal parenchyma and vessels facilitates surgery and reduces intra- and postoperative rates of complications, particularly in patients who previously underwent nephrectomy for renal cell carcinoma with carcinoma in the remnant kidney. In these patients, it is critical to show the possibility of performing conservative surgery, which avoids the need for life-long dialysis. In conclusion, high-resolution MDCT represents a further improvement in the preoperative evaluation of renal cell carcinoma.
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