June 2009, VOLUME 192
NUMBER 6

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June 2009, Volume 192, Number 6

Genitourinary Imaging

Original Research

Renal Cell Carcinoma: T1 and T2 Signal Intensity Characteristics of Papillary and Clear Cell Types Correlated with Pathology

+ Affiliations:
1Department of Radiology, Division of Abdominal Imaging and Intervention, Brigham and Women's Hospital, 75 Francis St., Boston, MA 02115.

2Department of Pathology, Brigham and Women's Hospital, Boston, MA.

3Department of Radiology, Hospital das Clinicas, Universidade de São Paulo, São Paulo, Brazil.

Citation: American Journal of Roentgenology. 2009;192: 1524-1530. 10.2214/AJR.08.1727

ABSTRACT
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OBJECTIVE. The objective of our study was to describe the T1 and T2 signal intensity characteristics of papillary renal cell carcinoma (RCC) and clear cell RCC with pathologic correlation.

MATERIALS AND METHODS. Of 539 RCCs, 49 tumors (21 papillary RCCs and 28 clear cell RCCs) in 45 patients were examined with MRI. Two radiologists retrospectively and independently assessed each tumor's T1 and T2 signal intensity qualitatively and quantitatively (i.e., the signal intensity [SI] ratio [tumor SI / renal cortex SI]). Of the 49 tumors, 37 (76%) were assessed for pathology features including tumor architecture and the presence of hemosiderin, ferritin, necrosis, and fibrosis. MRI findings and pathology features were correlated. Statistical methods included summary statistics and Wilcoxon's rank sum test for signal intensity, contingency tables for assessing reader agreement, concordance rate between the two readers with 95% CIs, and Fisher's exact test for independence, all stratified by RCC type.

RESULTS. Papillary RCCs and clear cell RCCs had a similar appearance and signal intensity ratio on T1-weighted images. On T2-weighted images, most papillary RCCs were hypointense (reader 1, 13/21; reader 2, 14/21), with an average mean signal intensity ratio for both readers of 0.67 ± 0.2, and none was hyperintense, whereas most clear cell RCCs were hyperintense (reader 1, 21/28; reader 2, 17/28), with an average mean signal intensity ratio for both readers of 1.41 ± 0.4 (p < 0.05). A tumor T2 signal intensity ratio of ≤ 0.66 had a specificity of 100% and sensitivity of 54% for papillary RCC. Most T2 hypointense tumors exhibited predominant papillary architecture; most T2 hyperintense tumors had a predominant nested architecture (p < 0.05).

CONCLUSION. On T2-weighted images, most papillary RCCs are hypointense and clear cell RCCs, hyperintense. The T2 hypointense appearance of papillary RCCs correlated with a predominant papillary architecture at pathology.

Keywords: clear cell renal cell carcinoma, MRI, papillary renal cell carcinoma, renal cell carcinoma

Introduction
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The incidence of renal cell carcinoma (RCC) has increased by 126% in the United States since 1950 [1]. This rising trend has been observed worldwide also and is due, in part, to the increased incidental detection of renal tumors using sonography, CT, and MRI [13]. The largest increase in RCC has occurred among patients 70–89 years old who are imaged for other medical reasons [2]. Although the increased incidence of RCC has occurred across all clinical stages of the disease, the greatest increase has been observed in low-stage localized tumors [2, 3].

RCCs consist of a heterogeneous group of tumors, each with distinct histologic and clinical characteristics [4]. Clear cell RCC, the most prevalent type (70%), and papillary RCC (15–20%) comprise most of the common forms of RCC encountered in clinical practice [5, 6].

Differentiating among the RCC types can be useful for counseling patients on prognosis and individualizing treatment planning because therapeutic strategies may differ for patients with different types of RCC. Papillary RCC carries a more favorable prognosis than clear cell RCC [69]. The 5-year cancer-specific survival rate among patients with papillary RCC approaches 90%; in patients with clear cell RCC, it is approximately 70% [6]. Therefore, an imaging-based diagnosis of an incidentally discovered small (≤ 3 cm) papillary RCC may help physicians select a less invasive procedure, such as percutaneous ablation, instead of surgical resection [10, 11] or may prompt physicians to consider observation in lieu of treatment in patients with comorbidities or a limited life expectancy. It would be helpful, therefore, if imaging could be used to suggest the type of RCC and, in particular, to differentiate the papillary type from the clear cell type. Furthermore, the histopathologic basis for the MRI appearance of papillary RCC is controversial [7, 1215], and to our knowledge no prior study has correlated tumor signal intensity on MRI with pathology results using statistical analysis. Therefore, the purpose of this study was to describe the T1 and T2 signal intensity characteristics of papillary RCC and clear cell RCC with pathologic correlation.

Materials and Methods
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Patient Selection

We obtained approval from our institutional review board to conduct this study; patient informed consent was waived. A review of our institution's electronic pathology database for the period from January 2000 to October 2005 revealed 539 RCCs that were surgically removed or percutaneously biopsied. Of these cases, 49 tumors (21 papillary RCCs and 28 clear cell RCCs) in 45 patients (29 men, 16 women; age range, 39–89 years; mean age, 64 years) had been examined with MRI at our institution. Of these, 37 of the 49 (76%) RCCs (21 papillary type and 16 clear cell type) had pathology specimens available for review. Specimens were derived from surgical resection (n = 22), percutaneous fine-needle (20- to 25-gauge) aspiration biopsy (n = 8), or percutaneous large-needle (18-gauge) biopsy (n = 7). The mean time between tissue diagnosis and MRI was 2 months (range, 1–13 months). The mean diameter of the papillary RCCs on MRI (3.6 ± 1.9 [SD] cm) was not significantly different from that of the clear cell RCCs (4.6 ± 2.6 cm) (p > 0.05).

MRI Protocol

MRI was performed on a 1.5-T system (Signa, GE Healthcare). Imaging included an axial fat-suppressed T1-weighted spoiled gradient-echo sequence (TR range/TE, 260–435/4.2; flip angle, 75°; section thickness, 4–6 mm; gap, 1 mm; field of view, 34–40 cm) or a 3D fast-acquisition multiple-excitation spoiled gradient-echo sequence (TR range/TE range, 4.4–7.3/1.5–2.2; flip angle, 10°; section thickness, 2.5 mm [effective]; gap, 0 mm; field of view, 32–40 cm) before and after IV gadolinium administration. T2-weighted imaging was performed with a single-shot fast spin-echo sequence (1,200–2,500/87–92; number of echoes acquired per TR, 184–264; section thickness, 5 mm; gap, 1 mm; field of view, 32–40 cm).

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Fig. 1 MRI features of papillary (n = 21) and clear cell (n = 28) renal cell carcinomas (RCCs). Scatterplot of reader 1- and reader 2-calculated tumor-to-renal cortex signal intensity ratios shows that signal intensity ratio of papillary RCC is statistically lower than that for clear cell RCC on T2-weighted images.

MRI Features

Two radiologists, using a PACS workstation with a monitor resolution of 1,280 × 1,024 pixels, assessed independently the T1 and T2 signal intensity of each tumor. Using a qualitative assessment based on visual inspection, the signal intensity of tumors on both T1- and T2-weighted images was classified as homogeneous or heterogeneous and as hypointense, isointense, hyperintense, or without a predominant signal intensity relative to normal renal cortex. Quantitative assessment was performed by obtaining region-of-interest measurements of tumor signal intensity and normal renal cortex signal intensity. A tumor signal intensity ratio was calculated by dividing tumor signal intensity by renal cortex signal intensity (SI): (tumor SI / renal cortex SI). The mean and one-quartile signal intensity ratios were used to calculate sensitivity and specificity. Enhanced images were not assessed because it is well established in the literature that papillary RCCs are hypovascular compared with clear cell RCCs [5, 13, 1619] and because our purpose was to evaluate T1 and T2 signal characteristics of papillary and clear cell RCCs and correlate their appearances with pathology results.

Pathologic Features

A single pathologist reviewed all specimens without knowledge of the imaging findings and classified each tumor as papillary or clear cell RCC according to the revised classification of renal tumors [4, 20, 21]. For each tumor, the following pathology characteristics were scored: tumor cellularity (low, intermediate, or high), nucleus-to-cytoplasm ratio (low, < 1:1; intermediate, 1:1; or high, > 1:1), and tumor cell architecture (papillary, nested, solid, cystic, or tubular). The presence or absence of hemosiderin, ferritin, fresh blood, calcification, necrosis, and fibrosis was documented.

Statistical Analysis

Stratified analyses of the two types of RCC were conducted. For categorical variables, contingency tables were constructed between the classifications by the two readers. The analysis of proportions and Fisher's exact test of independence were performed to compare the readings of the readers.

For continuous variables, summary statistics were reported using means ± SDs; Wilcoxon's rank sum tests were performed to compare the median values of the signal intensity, and the Student's t test was used to compare the mean values. Statistical significance was reached when p ≤ 0.05. Imaging features and pathology findings were correlated.

Interobserver agreement was calculated using the concordance rate, defined as the ratio between the sum of the diagonal counts and the sample size, stratified by T1 or T2 signal intensity and by RCC type. The associated 95% CIs were computed for the concordance rates.

Spearman's correlation coefficient was computed among the variables. It represents a variable degree of correlation including perfectly negative (r = –1.0), strongly negative (r = –0.8), moderately negative (r = –0.5), weakly negative (r = –0.2), perfectly positive (r = 1.0), strongly positive (r = 0.8), moderately positive (r = 0.5), weakly positive (r = 0.2), or not present (r = 0.0) [22].

Results
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MRI Features

On T1-weighted images (Table 1), the results of qualitative assessment of tumor signal intensity were variable. Using quantitative assessment, the tumor signal intensity ratios on T1-weighted images were similar for the two RCC types. The mean tumor T1 signal intensity ratios of papillary RCCs (reader 1, 0.86 ± 0.23; reader 2, 0.82 ± 0.30) were not significantly different from those of clear cell RCCs (reader 1, 0.81 ± 0.15; reader 2, 0.84 ± 0.27).

TABLE 1: MRI Features of Papillary and Clear Cell Renal Cell Carcinomas (RCCs): Qualitative Assessment of T1 and T2 Signal Intensity

On T2-weighted images (Table 1), qualitative assessment indicated that most papillary RCCs were homogeneously or heterogeneously hypointense and that most clear cell RCCs were either homogeneously or heterogeneously hyperintense (p < 0.01). None of the clear cell RCCs was hypointense when classified by reader 1 and only one was hypointense when assessed by reader 2. None of the papillary RCCs was hyperintense. Quantitative assessment showed a lower T2 signal intensity ratio for papillary RCCs compared with clear cell RCCs (Fig. 1). The mean T2 signal intensity ratios of papillary RCCs (reader 1, 0.65 ± 0.20; reader 2, 0.69 ± 0.16) were significantly less than those of clear cell RCCs (reader 1, 1.48 ± 0.48; reader 2, 1.34 ± 0.46) (p = 0.01).

Pathology Features

There was a predominance of papillary architecture among the papillary RCCs (16/21), and a nested architecture was seen for most clear cell RCCs (11/16) (Table 2). Tumor cellularity and nucleus-to-cytoplasm ratio were similar for the two RCC types. There were no statistically significant differences between papillary RCC and clear cell RCC regarding the presence of hemosiderin, ferritin, fresh blood, necrosis, fibrosis, or calcification.

TABLE 2: Pathology Findings of Papillary and Clear Cell Renal Cell Carcinomas (RCCs)

Correlation Between MRI Features and Pathology Features

On T1-weighted images, statistical analyses of qualitative assessment of MRI features evaluated by reader 1 only and pathology (Table 3) showed a predominance of high cellularity among heterogeneous tumors (10/12) (p = 0.04). There was no correlation between tumor signal intensity and nucleus-to-cytoplasm ratio; predominant tumor architecture; or presence of hemosiderin, fresh blood, necrosis, fibrosis, or calcification. Ferritin was present in only two tumors and they both were heterogeneous (p = 0.04). The analysis results of reader 2 for T1-weighted images were similar to those of reader 1, and there were no statistically significant differences between tumor T1 signal intensity and pathology features.

TABLE 3: Correlation Between T1-Weighted MRI Features of Papillary and Clear Cell Renal Cell Carcinomas (RCCs) and Pathology Findings

On T2-weighted images (Table 4), qualitative assessment of tumor signal intensity correlated with a predominant architecture: Papillary architecture correlated with hypointense tumors (reader 1, 11/12; reader 2, 9/10) (Fig. 2A, 2B), and nested architecture correlated with hyperintense tumors (reader 1, 4/6; reader 2, 5/7) (Fig. 3A, 3B) (p < 0.05). None of the tumors that were hyperintense had predominant papillary architecture. For reader 2 only, heterogeneous signal intensity correlated with the presence of necrosis (p = 0.03). There was no correlation between tumor T2 signal intensity and cellularity; nucleus-to-cytoplasm ratio; or the presence of hemosiderin, ferritin, fresh blood, fibrosis, or calcification.

TABLE 4: Correlation Between T2-Weighted MRI Features of Papillary and Clear Cell Renal Cell Carcinomas (RCCs) and Pathology Findings

Sensitivity and Specificity of T2 Tumor Signal Intensity

Qualitative assessment of tumor T2 signal intensity was correlated with pathology type. Hypointense tumors had a specificity of 100% and 96% (readers 1 and 2, respectively) and a sensitivity of 58% and 46% (readers 1 and 2, respectively) for papillary type. For both readers, hyperintense tumors on T2-weighted images had a specificity of 100% and a sensitivity of 36% for clear cell RCC.

Quantitative assessment of tumor T2 signal intensity was also correlated with pathology type. On T2-weighted images, a tumor signal intensity ratio of ≤ 0.93 (median) had a specificity of 86% and sensitivity of 96% for papillary RCC; a tumor signal intensity ratio of ≤ 0.66 (one quartile) had a specificity of 100% and a sensitivity of 54% for papillary RCC.

Interobserver Agreement

Concordance between the two readers for the qualitative assessments varied. Concerning the T1 signal intensity, the concordance rates between the readers were 50% (95% CI, 31.5–68.5%) for clear cell RCC and 47.6% (26.3–69.0%) for papillary RCC. Concerning the T2 signal intensity, the concordance rates between the readers were 71.4% (55.0–88.2%) for clear cell RCC and 66.7% (46.5–86.8%) for papillary RCC. When using quantitative assessment, concordance was better and varied from moderately to perfectly positive regarding signal intensity measurements on T1-weighted images (r = 0.6) and T2-weighted images (r = 0.9).

Discussion
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Our study describes the T1 and T2 MRI features of the papillary and clear cell types of RCC and analyzes the pathologic basis for their MRI appearances. On T2-weighted images, a hypointense tumor was typical of papillary RCC; T2 hyperintensity was seen only among the clear cell RCCs. Others have also described papillary RCCs as typically T2 hypointense [1215, 23] and clear cell RCCs as T2 hyperintense [13, 15, 18]. However, to our knowledge, none has reported the sensitivity and specificity of T2 tumor signal intensity to differentiate papillary RCC from clear cell RCC. Furthermore, no studies have statistically correlated the MRI features of papillary and clear cell RCCs with pathology findings. In addition, in previous reports, investigators have included only subjective assessments of tumor signal intensity [1215]. We found moderate to high concordance between the two readers' subjective assessments. However, the measurements of tumor signal intensity used in our study were more reproducible than subjective assessments, as shown by a higher interobserver agreement. We found that the T2 signal intensity (SI) ratio (tumor SI / renal cortex SI) of ≤ 0.66 had a specificity of 100% for papillary RCC. Therefore, in clinical practice, a small renal tumor that has a T2 signal intensity ratio of ≤ 0.66 is unlikely to represent clear cell RCC but could represent papillary RCC.

Other solid renal tumors also can be T2-hypointense, such as angiomyolipoma with minimal fat and solitary fibrous tumor of the kidney [24]. Solitary fibrous tumor of the kidney is usually a well-circumscribed solid mass attached to the renal capsule without necrosis or hemorrhage [24]. Although it is not known how to distinguish these tumors from RCC, they are extremely rare. Angiomyolipoma with minimal fat is a more common neoplasm: Approximately 4–5% of angiomyolipomas contain little or no fat [25]. Relative to RCC, angiomyolipoma with minimal fat has been shown to have a higher signal intensity index and lower tumor-to-spleen signal intensity ratio on double-echo chemical shift MRI [26]. The signal intensity index was calculated as follows: where TSIin is tumor signal intensity on in-phase images and TSIopp is tumor signal intensity on opposed-phase images. The tumor-to-spleen ratio was calculated as follows: where SSIopp is spleen signal intensity on opposed-phase images and SSIin is spleen signal intensity on in-phase images [26]. That study showed that angiomyolipoma with minimal fat can be differentiated from RCC when the signal intensity index is greater than 25% and the tumor-to-spleen ratio is ≤ –32%, with a specificity of 93% and 97%, respectively [26]. The signal intensity index and the tumor-to-spleen ratio likely reflected the small amount of fat cells in the angiomyolipomas evaluated in their study, but more data are needed to validate whether these parameters can be used to reliably differentiate angiomyolipoma with minimal fat from RCC. Furthermore, although these parameters can be used to favor a diagnosis of angiomyolipoma relative to RCC, when a T2 hypointense enhancing renal mass is encountered, papillary RCC, angiomyolipoma with minimal fat, and conceivably solitary fibrous tumor cannot be diagnosed definitively, and percutaneous biopsy may be needed [27]. Conversely, when a small T2 hyperintense renal neoplasm is encountered, the clear cell type of RCC is strongly favored.

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Fig. 2A 57-year-old man with 3.6-cm type 1 papillary renal cell carcinoma (RCC). On T2-weighted MR image, both readers classified tumor as hypointense. Tumor signal intensity ratio was 0.36 for reader 1 and 0.45 for reader 2.

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Fig. 2B 57-year-old man with 3.6-cm type 1 papillary renal cell carcinoma (RCC). Photomicrograph of pathology specimen shows papillary RCC has papillary architecture. There was no hemosiderin, ferritin, fibrosis, necrosis, or calcification.

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Fig. 3A 89-year-old man with 2.6-cm clear cell renal cell carcinoma (RCC). On T2-weighted MR image, both readers classified tumor as hyperintense. Tumor signal intensity ratio was 2.00 for reader 1 and 1.60 for reader 2.

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Fig. 3B 89-year-old man with 2.6-cm clear cell renal cell carcinoma (RCC). Photomicrograph of pathology specimen shows clear cell RCC has nested architecture.

In prior reports, investigators postulated that papillary RCC is T2 hypointense because of the presence of hemosiderin [7, 1215]. Others have suggested that papillary RCC is T2 hypointense because of the presence of ferritin [12]; fresh blood [12, 15]; fibrosis, calcifications, or a high nucleus-to-cytoplasm ratio [12]. Indeed, iron-containing substances such as hemosiderin and ferritin would be expected to decrease T2 signal intensity. However, our study showed that only the presence of a predominantly papillary architecture on pathology correlated with a T2 hypointense appearance on MRI. The presence of a fibrovascular stalk, the hallmark of a papillary architecture [4], might explain this appearance because fibrous tissue is usually T2 hypointense [28]. However, further studies are necessary to confirm this hypothesis.

Our study is limited in that chemical shift gradient-echo images were not assessed. Chemical shift imaging can be used to differentiate angiomyolipomas that contain abundant amounts of fat cells from RCCs [29]. In addition, it has been suggested that, excluding angiomyolipoma, loss of signal on out-of-phase images can be used to favor the diagnosis of clear cell RCC; this finding has been ascribed to intratumoral lipid found in clear cell RCC [30]. However, more recently, signal loss on out-of-phase images was observed as frequently in papillary RCC as in clear cell RCC [23]. That study also showed that some papillary RCCs had a low signal intensity on in-phase images relative to its signal on out-of-phase images [23]. This finding was postulated to be due to the presence of hemosiderin and its magnetic susceptibility effect [23]. This postulate is reasonable, but in our study hemosiderin was found as frequently in clear cell RCC as in papillary RCC. Furthermore, because lipid and hemosiderin affect signal intensity in an opposite way (the former results in increased, and the latter results in decreased signal intensity on in-phase images relative to out-of-phase chemical shift images), the coexistence of these two substances within a voxel may cancel their effects [23]. Hence, the data are insufficient to conclude that chemical shift imaging can be used to differentiate clear cell RCC from papillary RCC. However, as discussed, chemical shift imaging may be useful in distinguishing angiomyolipoma from RCC and therefore is useful in clinical practice [29].

Another limitation of our study is that the pathology analysis relied on biopsy specimens in 15 of the 37 cases and, therefore, did not include the entire tumor. As a result, some portions of tumor were not evaluated in those cases. However, percutaneous biopsy was performed before ablation, so the entire tumor could not be examined. Because most tumors were small, the biopsy sample is likely representative. Furthermore, our study did not include other types of RCC, such as chromophobe RCC, collecting duct RCC, and medullary RCC, but these tumors are rare. Nevertheless, these data cannot be used to differentiate clear cell RCC or papillary RCC from those other types. Finally, the tumor signal intensity ratio may vary depending on the MRI parameters used and, therefore, may not be applicable with different pulse sequences. Further study is necessary to assess how the signal intensity ratio varies with different pulse sequence parameters.

In conclusion, small papillary RCC is typically T2 hypointense and clear cell RCC is typically T2 hyperintense. When a T2 hypointense renal neoplasm in encountered in clinical practice, clear cell RCC is unlikely, and the differential diagnosis can be narrowed to include papillary RCC and other entities such as angiomyolipoma with minimal fat and the rare solitary fibrous tumor of the kidney. If imaging features cannot be used to differentiate them or if a tissue diagnosis is desired, percutaneous biopsy is warranted. When a small T2 hyperintense renal neoplasm is encountered, clear cell RCC is strongly favored. Contrary to prior reports, the T2 hypointense feature of papillary RCCs correlated only with predominantly papillary architecture, not with the presence of hemosiderin or other iron-containing materials.

Address correspondence to M. R. Oliva ().

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