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1 University Hospital of Strasbourg, Radiology B Chirugie A, Hopital Civil CHU,
1, place de l'hopital BP 426, Strasbourg, Cedex, France 67091.
2 University Hospital of Strasbourg, Hopital Civil–Urology, Strasbourg,
Cedex, France 67091.
Received February 21, 2004;
accepted after revision June 14, 2004.
Abstract
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MATERIALS AND METHODS. Eighty tumors (73 renal cell carcinomas [RCCs] and seven oncocytomas) were preoperatively evaluated by MRI. MRI findings were assessed with a special focus on perinephric fat and pseudocapsule. Correlations were performed with pathologic staging after surgery.
RESULTS. At pathology, a pseudocapsule was recognized in 79 cases. Twenty-three RCC were staged pT3a (21 clear cell; two papillary). MR images exhibited a pseudocapsule in 90% of cases as a hypointense rim surrounding the tumor on T2-weighted images. MRI findings concerning isolated analysis of the pseudocapsule for differentiating stage T1/T2 from T3a were sensitivity: 86%, 50%; specificity: 95%, 92%; positive predictive value: 95%, 33%; negative predictive value: 88%, 92%; and accuracy: 93%, 89%, for clear cell and papillary types, respectively. For stage T3a, with both abnormalities of the pseudocapsule and perirenal fat, results were, for overall RCC sensitivity: 84%; specificity: 95%; positive predictive value: 91%; negative predictive value: 91%; and accuracy: 91%.
CONCLUSION. The identification of the pseudocapsule offers an additional value for local staging by MRI. The presence of an intact pseudocapsule is a sign of lack of perinephric fat invasion. It is more likely to predict that the tumor can be removed by partial surgery.
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In the early reports of MRI, the presence of a hypointense rim surrounding RCCs corresponding to a so-called "pseudocapsule" was recognized [6–8]. It seems to be a pathologic feature frequently seen in the early stages. The identification of a pseudocapsule has been proposed as a sign for a localized intrarenal lesion so that partial nephrectomy could be indicated when an intact pseudocapsule is detected. However the meaning of this imaging feature has not yet been clearly established.
The purpose of this study was to analyze the role of MRI in showing the presence of a pseudocapsule in renal tumors, and to determine its significance and implication for the local staging of renal masses.
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MRI Study Protocol
MR imaging was performed using 1.0 T MRI unit (Intera NT, Philips Medical
Systems). The MRI sequences and their parameters were as follows: axial
T1-weighted SE (TR/TE: 350/16, 2 excitations, field of view: 350 x 380,
matrix size: 256 x 512, acquisition time: 2 min 44 sec), and fast
spin-echo T2-weighted axial (TR/TE: 1800/150eff msec, turbo factor: 64, 3
accumulations, field of view: 350 x 380, matrix size: 256 x 512,
acquisition time: 1 min 32 sec). All sequences were obtained with a slice
thickness of 5 mm and a gap of 1 mm. An additional coronal fat-suppressed fast
spin-echo T2-weighted image was performed for more precise evaluation and
localization of the lesions.
After the imaging was completed, an axial dynamic breath-hold gadolinium-enhanced 2D spoiled gradient-refocused echo (GRE) sequence (TR/TE: 85/1.6 msec, flip: 70°, field of view: 350 x 380, one accumulation; matrix: 256 x 512, time of acquisition: 12 sec) was obtained. After an unenhanced acquisition, this sequence was repeated six times, with 30 sec interimaging delay at 30 sec, 60 sec, 90 sec, 120 sec, 180 sec, and 300 sec, at the end of a rapid manual injection of gadopentetate dimeglumine (0.1 mmol/kg body weight; Magnevist, Schering). Finally, axial delayed postcontrast breath-hold fat-suppressed T1-GRE images were obtained as the final sequence. Overall examination time was between 30 and 40 min.
Imaging Analysis
All images were retrospectively and independently reviewed by two senior
radiologists who were unaware of the surgical and pathologic findings. A third
radiologist was used for consensus when the two others did not agree (11
cases). The tumor diameter was measured in three planes and the largest
measurement was considered as the tumor size. Attention was given to the
following points: tumor signal intensity compared with normal renal
parenchyma, recognition of a pseudocapsule, and presence of perirenal fat
infiltration.
The pseudocapsule was defined as a thin linear regular hypointense band on T2- and T1-weighted images surrounding the tumor. Patients were staged according to criteria based on the recent modified TNM classification that separates tumors confined to renal capsule of 7 cm or less in diameter (T1) from those equal to or greater than 7 cm in diameter (T2). We considered on MRI as stage T1 or T2 when there was a regular continuous thin rim surrounding the lesion and lack of infiltration of the perirenal fat or a regular margin mass without infiltration of the perirenal fat (as defined in TNM staging) and without visualization of a complete thin rim or a lesion with an intact regular rim but an infiltrative aspect (stranding) of the perinephric fat. The stage T3a is defined in terms of tumor spread to the perinephric fat, but confined to Gerota's fascia [8].
On MR images, the pattern for staging T3a was determined by the presence of
perinephric thick streaks and/or nodules (
5 mm in size) surrounding the
lesion and extending into the perirenal fat and any type of disruption of this
rim or no rim identified, on both T2- and T1-weighted images.
MRI results were compared with surgical findings and pathologic examination including both macroscopic and microscopic analysis with a thorough correlation between characteristics of the pseudocapsule on images and pathology.
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Data comprised 73 RCCs of clear cell type (CC RCC) in 44 cases and papillary type in 29 cases. Seven patients had a unique oncocytoma.
At pathology, a pseudocapsule was described in 79 cases. It was absent in
one case (of oncocytoma). This pseudocapsule was intact in 52 cases, and
disrupted in 27 cases (26 RCC, one oncocytoma). Twenty-three tumors were
established to be stage pT3a (21 CC RCC, 2 papillary type). Among them, two CC
RCC had minor focal invasion of perirenal fat. The characteristics of the
pseudocapsule were different in composition. The outer margin, concerning the
exophytic part of the tumor hanging off the kidney, was a fibrous surrounding
rim with focal bulging, in continuity with the normal fibrous band of the
renal capsule. It was associated with reactive hyperplasia in nine cases. The
inner margin concerned the part in contact with the parenchyma. It was
composed of thick compressed renal parenchyma with few fibrous elements and
some infiltrating neoplastic cells in normal parenchyma in 12 cases. In nine
cases, an organized fibrous band entirely surrounded the lesion, especially in
the inner part of tumor. An absent or disrupted external fibrous band was
found in 23 cases of CC RCC and in 3 cases of the papillary type. All tumors
with an intact fibrous band had a low grade (1 or 2) and were 
4 cm in
diameter.
At MR imaging, the T1-weighted signal intensity of CC RCC was variable: hyperintense (eight cases), isointense (five cases), hypointense (31 cases) and always hyperintense and heterogeneous on T2-weighted imaging (Figs. 1A, 1B, 2A, 2B, 2C, and 2D). For papillary tumors, 26 of 29 were hypointense and homogeneous on T2-weighted imaging, except for two cases (Fig. 3). Three patients had a more heterogeneous pattern but with a large hypointense zone (Figs. 4A and 4B).
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On MR images, 72 of 80 lesions (90%) exhibited typical pseudocapsule as a hypointense rim surrounding the tumor. The pseudocapsule was identified in 39 of 44 cases of CC RCC and in 27 of 29 of papillary type. It was seen as a hypointense rim on T1-weighted images in 37 cases (50%) and in 67 cases (92%) on T2-weighted images. It was found in 57 cases (78%) on contrast-enhanced T1-weighted images where it appeared with a slightly more intense signal than that of the tumor. All pseudocapsules detected on T1 sequence also were seen on the T2 sequence. They appeared as a complete or incomplete band on T2-weighted images (Table 1).
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On the MR images, if we consider only the isolated characteristics of the fibrous hypointense pseudocapsule (normal, disrupted, or absent), we found the results concerning staging for CC RCC to be 20 true-positive, one false-positive, three false-negative, and 22 true-negative cases (sensitivity: 86%, specificity: 95%, positive predictive value: 95%, negative predictive value: 88%; and accuracy 95%) and for the papillary type, one true-positive, one false-negative, two false-positive, and 25 true-negative cases (sensitivity: 50%, specificity: 92%, positive predictive value: 33%, negative predictive value: 92%; and accuracy: 89%) (Fig. 5). One false-negative of CC RCC was due to a microscopic extension crossing the fibrous rim. The two false-positive papillary types were explained by the absence of visualization of the pseudocapsule because of homogeneous major hypointensity of the tumor on T2-weighted sequence.
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On MR images, if only perinephric fat abnormalities were taken into account, as defined according to modified TNM stage T3a, results for CC RCCs were 19 true-positive, six false-positive, and two false-negative with an overall 17 true-negative patients, and for papillary type, one true-positive and one false-negative with 27 true-negative cases. That is for all types of our RCC sensitivity: 90%, specificity: 74%, positive predictive value: 76%, negative predictive value: 89%, and accuracy: 81%. Five of our false-positive results were due to inflammation in the perirenal space without any tumor invasion (Fig. 6). The other results could be explained by edema with collateral vessels. Our false-negative case concerned minimal invasion at pathology.
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On MR images, if we consider the association of abnormalities of the pseudocapsule and perirenal fat as criteria to diagnose stage T3a, results for CC RCC were 22 true-positive, 18 true-negative, one false-positive, and three false-negative (sensitivity: 91%, specificity: 97%, positive predictive value: 95%, negative predictive value: 96%, and accuracy: 95%) (Fig. 7), and for papillary type, 27 true-negative, one false-negative, and one false-positive (specificity: 96%, negative predictive value: 96%, and accuracy: 93%) (Table 2). For overall RCC, results were: sensitivity: 84%, specificity: 95%, positive predictive value: 91%, negative predictive value: 91%, and accuracy: 91% (Table 3).
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The hypointense rim was not exclusively seen in RCCs. The appearance of the oncocytomas was variable. All of them, except for one case, exhibited a fibrous hypointense band, which was found at pathology. All presented with a variable low signal intensity on T1-weighted images. They were more or less hyperintense heterogeneously on T2-weighted images. Only two exhibited a typical central scar. One oncocytoma presented with a disruption of the hypointense band and had irregularities in the perirenal fat, which was confirmed at pathology. If we consider staging for all 80 tumors, with assigning a stage to the oncocytomas, our results were even better with sensitivity: 85%, specificity: 96%, positive predictive value: 92%, negative predictive value: 92%, and accuracy: 92% (Table 3).
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Involvement of perirenal fat tissue represents a key point in treatment planning in modifying the surgical approach from conservative to radical nephrectomy. If partial nephrectomy is contemplated, it is essential to know preoperatively if the perinephric fat is or is not invaded by the tumor. Furthering the distinction and accurate differentiation of stage T3a of the TNM classification, from a therapeutic point of view, parenchyma-sparing surgery should be performed only when the tumor is confined to the kidney parenchyma and encapsulated so that is surrounded by a distinct pseudocapsule [2]. Even if this pseudocapsule is not described in the TNM classification, it may play a critical role in deciding on nephron-sparing surgery. RCCs generally do not have a true histologic capsule but usually possess a peripheral surrounding pseudocapsule composed of compressed normal renal parenchyma and fibrous tissue [8, 17–19]. This latter merges with dense fibrous septa that course through the neoplasm. When RCC grows, the fibrous tissue in the renal stroma is stimulated and also grows, surrounding the tumor and inhibiting further growth. The variation of the pseudocapsule thickness can be explained by different growth rates and varying locations of the tumor. In cases where RCC grows slowly, the fibrous tissue is thicker because of reactive hyperplasia. In cases where RCC grows fast, the fibrous tissue is thinner because of the shorter period of reactive hyperplasia. Encapsulated RCCs have been demonstrated to be small and of low histologic grade, slow growing, and less likely to metastasize [2, 20]. In some larger tumors, although tumor invasion is seen, a residual pseudocapsule can be found in some areas [17].
In cases of exophytic location where the tumor is growing outside the kidney, the outer and inner margins of this pseudocapsule differ in composition. The outer margin is formed by condensed fibrous tissue coming from reactive hyperplasia of the renal capsule and confused with it, and in certain cases associated compressed parenchyma. The inner part is composed of thick compressed normal renal parenchyma. In all of our cases, the outer margin was described by our pathologist as a fibrous rim around the tumor in continuity with the fibrous renal capsule surrounding renal parenchyma (Figs. 1A, 1B, 2A, 2B, 2C, and 2D). It was interpreted to be a segment of this perirenal capsule. After the neoplasm breaks off the renal capsule, direct tumor extension can occur in the perinephric fat [19]. According to the method described by Robson [2, 6, 21] on CT or MR images, the extracapsular spread to perinephric fat is classified as Robson stage II, whereas in stage I there is no evidence of perinephric fat invasion. Tumor extension beyond the pseudocapsule was reported when images showed infiltration of perirenal fat that had perinephric stranding and/or nodules in it. Helical CT, although widely accepted as the preferred imaging technique in patients with RCC, has some limitations, mainly concerning the difficulty in differentiating Robson stage I from II [22]. Under- and overstaging of perinephric invasion are the most common staging errors of CT [5]. Perinephric stranding does not reliably indicate tumoral spread and is found in about half of patients with localized intrarenal tumors. It also may be caused by edematous vascular engorgement and/or inflammation [5]. The only highly specific finding (98%) is the presence of an enhancing nodule or soft-tissue mass in the perinephric space but this sign has only 46% sensitivity [9, 23, 24]. The sensitivity of CT in detecting pseudocapsule is very low [5, 8, 25, 26].
On MRI, the low-intensity band called pseudocapsule separating the tumor from the kidney was first described by Hricak et al. in 1985 [6]. The pseudocapsule appears as a hypointense rim surrounding the tumor and interposed between the tumor and normal renal parenchyma or perirenal fat on both T1 and T2 sequences. The signal intensity has been attributed to fibrous tissue [27]. T2-weighted images were found to be the most sensitive sequence for detecting the pseudocapsule, interposed between the higher intensity of the tumor and normal renal parenchyma [20, 25, 28]. Our study confirms this. From the results comparing the MRI appearance and the pathologic findings, a close relationship was found between the low-intensity band and the construction of the pseudocapsule. This rim appears on MR images when the thickness is greater than 2 mm. Fibrous tissue presents as low-intensity on T2-weighted images because of the tissue's short T2 relaxation time. The T1 relaxation time of fibrous tissue is longer than that of the kidney but the signal intensity of compressed normal renal parenchyma is slightly higher because of the decreased liquid in it. In postcontrast T1-weighted images, the visualization of the pseudocapsule is inferior in relation to that of T2-weighted imaging. Because of its composition with fibrous tissue, its enhancement occurs later and its distinction from surrounding normal renal parenchyma is more difficult. Fat-suppressed T2-weighted images were not as pertinent to evaluation of the pseudocapsule because of lack of contrast due to hypointense perirenal space.
In opposition to Yamashita et al. [8], who have stated that the incidence of finding a pseudocapsule was related to size of the mass, we have found pseudocapsule in lesions smaller than 4 cm in diameter. In our study, the frequency of appearance of the pseudocapsule (90%) was clearly better than the results presented in the literature, which ranged from 54–66% [20, 25, 28]. This fact reflects differences in machine performance and recent technical improvements. Only three false-negative results were generated by a microscopic invasion not detected on MR images. As with all imaging techniques, it is extremely difficult with MRI to determine whether malignant tissue extends to adjacent normal tissue when strictly regular margins are found. Microscopic local invasion could have occurred. MRI was particularly accurate in identifying true-negative findings. However, our results were slightly less optimistic compared to those presented in the literature regarding true-negative findings for perinephric fat of 100% [28]. Therefore, the negative predictive value of MRI was rather high (96%) for detecting T3a disease. Specificity and positive predictive value also were highly significant if pseudocapsule assessment is considered as a part of our diagnosis. MRI had a pertinent accuracy for evaluating possible involvement of perinephric fat using the aspect of the pseudocapsule as an additional feature. Obviously, the analysis of the pseudocapsule offers an additional value to the efficiency of the method for local staging. This is particularly necessary to avoid false-positive results secondary to inflammation of perirenal fat (Fig. 5). None of our cases with continuous low-intensity pseudocapsule band presented tumor invasion of perirenal fat. The probability that perirenal fat has been infiltrated is lessened when the low-intensity band or rim appears on T2-weighted images even though the tumor has protruded into the perirenal fat capsule. Our true-negative results for papillary tumors were significantly better compared to those of CC RCC because the stage T3a is less frequent for this histologic type.
There are several limitations to the detection of a pseudocapsule by MRI. First, with hypointense tumors its detection may be less accurate on T2-weighted sequencing. We collected two false-positive results in our papillary tumors, explained by the typical lowintensity pattern of this histologic type and the lack of delineation of the surrounding rim. Second, if the tumor is small, partial volume averaging may obscure its visualization. The direct multiplanar imaging capabilities of MRI make tumor evaluation easy to do in three planes. Coronal, sagittal, or oblique views are required to avoid this phenomenon on the upper and lower part of the tumor. In our material, coronal views considerably assisted in defining the relationships of polar masses to the adjacent perirenal space. Third, a chemical shift artifact, observed at the interface between the tumor and the perinephric fat, forms another limitation and needs to be differentiated from the pseudocapsule. However, this artifact only is seen in the frequency direction encoding and not between the tumor and renal parenchyma. In our study, this artifact did not cause any error in our interpretation. We also mainly considered the T2-weighted aspect in a retrospective image review, but this sequence definitively had the best accuracy in showing the pseudocapsule.
As the pseudocapsule also was found in oncocytomas, it is not useful for differentiating RCC from this benign solid tumor. It cannot be used to predict the nature of the lesion.
In conclusion, our results confirm that identification of the pseudocapsule offers an additional value to the performance of preoperative MRI to stage renal tumors according to TNM classification. A routine T2-weighted sequence without fat suppression is the most useful sequence for showing this feature. Multiplanar T2-weighted MR sequences seem to be suited for making this determination. The presence of an intact pseudocapsule is a sign of lack of perinephric fat invasion. An intact pseudocapsule is more likely to predict that the tumor can be removed by nephron-sparing surgery.
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